1 Genomic diversity and global distribution of Saccharomyces … · 88 (Peris et al. 2014, 2016;...

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Genomic diversity and global distribution of Saccharomyces eubayanus, the wild ancestor of 1

hybrid lager-brewing yeasts 2

3

Quinn K. Langdon1, David Peris1,2,3, Juan I. Eizaguirre4, Dana A. Opulente1,2, Kelly V. Buh1, 4

Kayla Sylvester1,2, Martin Jarzyna1,2, María E. Rodríguez5, Christian A. Lopes5, Diego 5

Libkind4,@, Chris Todd Hittinger1,2,@ 6

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1Laboratory of Genetics, J. F. Crow Institute for the Study of Evolution, Wisconsin Energy 8

Institute, Genome Center of Wisconsin, University of Wisconsin-Madison, Madison, WI 53706, 9

USA 10

2DOE Great Lakes Bioenergy Research Center, University of Wisconsin-Madison, Madison, WI 11

53706, USA 12

3Department of Food Biotechnology, Institute of Agrochemistry and Food Technology (IATA), 13

CSIC, Valencia, Spain 14

4Laboratorio de Microbiología Aplicada, Biotecnología y Bioinformática de Levaduras, Instituto 15

Andino Patagónico de Tecnologías Biológicas y Geoambientales (IPATEC), Consejo Nacional 16

de Investigaciones, Científicas y Técnicas (CONICET)-Universidad Nacional del Comahue, 17

8400 Bariloche, Argentina 18

5Instituto de Investigación y Desarrollo en Ingeniería de Procesos, Biotecnología y Energías 19

Alternativas (PROBIEN, CONICET-UNCo), Neuquén, Argentina 20

@Corresponding authors: CTH [email protected] & DL [email protected] 21

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.CC-BY-NC 4.0 International licenseis made available under aThe copyright holder for this preprint (which was not peer-reviewed) is the author/funder. It. https://doi.org/10.1101/709535doi: bioRxiv preprint

https://doi.org/10.1101/709535

http://creativecommons.org/licenses/by-nc/4.0/

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Abstract: 24

S. eubayanus, the wild, cold-tolerant parent of hybrid lager-brewing yeasts, has a 25

complex and understudied natural history. The exploration of this diversity can be used both to 26

develop new brewing applications and to enlighten our understanding of the dynamics of yeast 27

evolution in the wild. Here, we integrate whole genome sequence and phenotypic data of 200 S. 28

eubayanus strains, the largest collection to date. S. eubayanus has a multilayered population 29

structure, consisting of two major populations that are further structured into six subpopulations. 30

Four of these subpopulations are found exclusively in the Patagonian region of South America; 31

one is found predominantly in Patagonia and sparsely in Oceania and North America; and one is 32

specific to the Holarctic ecozone. S. eubayanus is most abundant and genetically diverse in 33

Patagonia, where some locations harbor more genetic diversity than is found outside of South 34

America. All but one subpopulation shows isolation-by-distance, and gene flow between 35

subpopulations is low. However, there are strong signals of ancient and recent outcrossing, 36

including two admixed lineages, one that is sympatric with and one that is mostly isolated from 37

its parental populations. Despite S. eubayanus’ extensive genetic diversity, it has relatively little 38

phenotypic diversity, and all subpopulations performed similarly under most conditions tested. 39

Using our extensive biogeographical data, we constructed a robust model that predicted all 40

known and a handful of additional regions of the globe that are climatically suitable for S. 41

eubayanus, including Europe. We conclude that this industrially relevant species has rich wild 42

diversity with many factors contributing to its complex distribution and biology. 43

44

45

46


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Introduction: 47

In microbial population genomics, the interplay of human association and natural 48

variation is still poorly understood. The genus Saccharomyces is an optimal model to address 49

these questions for eukaryotic microbes, as it contains both partly human-associated species (i.e. 50

Saccharomyces cerevisiae) and mostly wild species (e.g. Saccharomyces paradoxus). These two 51

examples also illustrate the complexity of studying yeast population genomics. Much of S. 52

cerevisiae population structure is admixed, and several lineages show signatures of 53

domestication (Liti et al. 2009; Schacherer et al. 2009; Gallone et al. 2016; Gonçalves et al. 54

2016). In contrast, S. paradoxus is almost exclusively found in the wild and has a population 55

structure that is correlated with geography (Leducq et al. 2014; Eberlein et al. 2019). Pure 56

isolates of their more distant relative Saccharomyces eubayanus have only ever been isolated 57

from wild environments; yet, hybridizations between S. cerevisiae and S. eubayanus were key 58

innovations that enabled cold fermentation and lager brewing (Libkind et al. 2011; Gibson and 59

Liti 2015; Hittinger et al. 2018; Baker et al. 2019). Other hybrids with contributions from S. 60

eubayanus have been isolated from industrial environments (Almeida et al. 2014; Nguyen and 61

Boekhout 2017), indicating that this species has long been playing a role in shaping many 62

fermented products. This association with both natural and domesticated environments makes S. 63

eubayanus an excellent model where both wild diversity and domestication can be investigated. 64

Since the discovery of S. eubayanus in Patagonia (Libkind et al. 2011), this species has 65

received much attention, both for brewing applications and understanding the evolution, ecology, 66

population genomics of the genus Saccharomyces (Sampaio 2018). In the years since its 67

discovery, many new globally distributed isolates have been found (Bing et al. 2014; Peris et al. 68

2014; Rodríguez et al. 2014; Gayevskiy and Goddard 2016; Peris et al. 2016; Eizaguirre et al. 69


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2018). Prior research has suggested that S. eubayanus is most abundant and diverse in the 70

Patagonian region of South America, where there are two major populations (Patagonia 71

A/Population A/PA and Patagonia B/Population B/PB) that recent multilocus data suggested are 72

further divided into five subpopulations (PA-1, PA-2, PB-1, PB-2, and PB-3) (Eizaguirre et al. 73

2018). There are two early-diverging lineages, West China and Sichuan, which were identified 74

through multilocus data (Bing et al. 2014) and whose sequence divergences relative to other 75

strains of S. eubayanus are nearly that of currently recognized species boundaries (Peris et al. 76

2016; Sampaio and Gonçalves 2017; Naseeb et al. 2018). A unique admixed lineage has been 77

found only in North America, which has approximately equal contributions from PA and PB 78

(Peris et al. 2014, 2016). Other isolates from outside Patagonia belong to PB, either the PB-1 79

subpopulation that is also found in Patagonia (Gayevskiy and Goddard 2016; Peris et al. 2016), 80

or a Holarctic-specific subpopulation that includes isolates from Tibet and from North Carolina, 81

USA (Bing et al. 2014; Peris et al. 2016). This Holarctic subpopulation includes the closest 82

known wild relatives of the S. eubayanus subgenomes of lager-brewing yeasts (Bing et al. 2014; 83

Peris et al. 2016). 84

To explore the geographic distribution, ecological niche, and genomic diversity of this 85

industrially relevant species, here, we present an analysis of whole genome sequencing data for 86

200 S. eubayanus strains. This dataset confirms the previously proposed population structure 87

(Peris et al. 2014, 2016; Eizaguirre et al. 2018) and extends the analysis to fully explore genomic 88

diversity. Even though S. eubayanus is genetically diverse and globally distributed, there are not 89

large phenotypic differences between subpopulations. This genomic dataset includes evidence of 90

gene flow and admixture in sympatry, as well as admixture in parapatry or allopatry. While S. 91

eubayanus has a well-differentiated population structure, isolation by distance occurs within 92


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subpopulations that are found globally, as well as within subpopulations restricted to a handful of 93

locations. Much of the genetic diversity is limited to northern Patagonia, but modeling suggests 94

that there are more geographic areas that are climatically suitable for this species, including 95

Europe. S. eubayanus maintains genetic diversity over several dimensions, including multiple 96

high-diversity sympatric populations and a low-diversity widespread invasive lineage. The 97

diversity and dispersal of this eukaryotic microbial species mirror observations in plants and 98

animals, including humans, which shows how biogeographical and evolutionary forces can be 99

shared across organismal sizes, big and small. 100

101

Results: 102

Global and regional S. eubayanus population structure and ecology: 103

To expand on existing data (Libkind et al. 2011; Bing et al. 2014; Peris et al. 2014; 104

Rodríguez et al. 2014; Gayevskiy and Goddard 2016; Peris et al. 2016; Eizaguirre et al. 2018), 105

we sequenced the genomes of 174 additional strains of S. eubayanus, bringing our survey to 200 106

S. eubayanus genomes. This large collection provides the most comprehensive dataset to date for 107

S. eubayanus. We note that the dataset does not contain West China or Sichuan strains (Bing et 108

al. 2014), which were unavailable for study and may constitute a distinct species or subspecies. 109

These strains were globally distributed (Figure 1A), but the majority of our strains were from 110

South America (172 total, 155 newly sequenced here). The next most abundant continent was 111

North America with 26 strains (19 new to this publication). We also analyzed whole genome 112

sequence data for the single strain from New Zealand (Gayevskiy and Goddard 2016) and the 113

single Tibetan isolate with available whole genome sequence data (Bing et al. 2014; Brouwers et 114

al. 2019). The collection sites in South America span from northern Patagonia to Tierra del 115


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Fuego (Figure 1B), while the North American isolates have been sparsely found throughout the 116

continent, including the Canadian province of New Brunswick and the American states of 117

Washington, Wisconsin, North Carolina, and South Carolina (Figure 1C). 118

119

Figure 1. S. eubayanus distribution and population structure. 120 S. eubayanus has a global distribution and two major populations with six subpopulations. (A) Isolation 121 locations of S. eubayanus strains included in the dataset. For visibility, circle size is not scaled by the 122 number of strains. Subpopulation abundance is shown as pie charts. The Patagonian sampling sites have 123 been collapsed to two locations for clarity. Details of sites and subpopulations found in South America 124 (B) and North America (C) with circle size scaled by the number of strains. (D) Whole genome PCA of S. 125 eubayanus strains and five hybrids with large contributions from S. eubayanus. (E) PCA of just PA. (F) 126 PCA of just PB and hybrid S. eubayanus sub-genomes. Color legends in A and D apply to this and all 127 other figures. 128 129 To determine population structure, we took several approaches, including Principal 130

Component Analysis (PCA) (Jombart 2008), phylogenomic networks (Huson and Bryant 2006), 131

and STRUCTURE-like analyses (Lawson et al. 2012; Raj et al. 2014). All methods showed that 132

S. eubayanus has two large populations that can be further subdivided into a total of six non-133

25

30

35

40

45

50

−120 −100 −80 −60Longitude

Latitude

PB−1

PB−2

PB−3Holarctic

PA−1 PA−2

NoAm

SoAm

−150

−100

−50

0

50

−100 0 100 200PC1 = 40.06%

PC2

= 9.

95%

PA−1

PA−2

PB−1

PB−2

PB−3

Holarctic

Hybrid

NoAm

SoAm

PA−1PA−2

−75

−50

−25

0

25

50

−150 −100 −50 0 50PC1 = 41.56%

PC2

= 7.

81%

PA−1

PA−2

−50

0

50

−100 0 100 200Longitude

Latitude

PA−1PA−2

PB−1PB−2

PB−3Holarctic

NoAmSoAm

−55

−50

−45

−40

−75 −70 −65 −60Longitude

Latitude

B

C

E

D

A

PB1

PB−2

PB−3

Holarctic−50

0

50

−50 0 50 100PC1 = 19.03%

PC2

= 13

.96%

PB−1

PB−2

PB−3

Holarctic

Hybrid

F


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admixed subpopulations and one abundant North American admixed lineage (Figure 1D and 134

Figure S1). We previously described the two major populations, PA and PB-Holarctic (Peris et 135

al. 2014, 2016), as well as the subpopulations PA-1, PA-2, PB-1, PB-2, Holarctic, and the North 136

American admixed lineage (Peris et al. 2016). PB-3 had been suggested by multilocus data 137

(Eizaguirre et al. 2018), and our new analyses confirm this subpopulation with whole genome 138

sequence data. All of the strains isolated from outside of South America belonged to either the 139

previously described North American admixed lineage (NoAm) or one of two PB 140

subpopulations, PB-1 or Holarctic. This dataset included novel PB-1 isolates from the states of 141

Washington (yHRMV83) and North Carolina (yHKB35). Unexpectedly, from this same site in 142

North Carolina, we also obtained new isolates of the NoAm admixed lineage (Figure 1C and 143

Table S1), and we obtained additional new NoAm strains in South Carolina. Together, with the 144

North Carolina strains reported here and previously (Peris et al. 2016), this region near the Blue 145

Ridge Mountains harbors three subpopulations or lineages, PB-1, Holarctic, and NoAm. We 146

were also successful in re-isolating the NoAm lineage from the same Wisconsin site, sampling 147

two years later than what was first reported (Peris et al. 2014) (Table S1), indicating that the 148

NoAm admixed lineage is established, not ephemeral, in this location. Additionally, we found 149

one novel South American strain that was admixed between PA (~45%) and PB (~55%) (Figure 150

1D “SoAm”). This global distribution and the well-differentiated population structure of S. 151

eubayanus is similar to what has been observed in S. paradoxus (Leducq et al. 2014, 2016) and 152

Saccharomyces uvarum (Almeida et al. 2014). 153

S. eubayanus has been isolated from numerous substrates and hosts, and our large dataset 154

afforded us the power to analyze host and substrate association by subpopulation. We found that 155

PA-2 was associated with the seeds of Araucaria araucana (45.71% of isolates, p-val = 6.11E-156


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07, F-statistic = 15.29). Interestingly, while PB-1 was the most frequently isolated subpopulation 157

(34% of isolates), it has never been isolated from A. araucana seeds. Instead, PB-1 was 158

associated with Nothofagus antarctica (52.31% of isolates, p-val = 0.017, F-statistic = 3.10). PB-159

1 was also the subpopulation isolated the most from Nothofagus dombeyi (75% of isolates from 160

this tree species), which is a common host of S. uvarum (Libkind et al. 2011; Eizaguirre et al. 161

2018). PB-2 was positively associated with Nothofagus pumilio (36.59% of isolates, p-val = 9.60 162

E-04, F-statistic = 6.59), which could be an ecological factor keeping PB-2 partly isolated from 163

its sympatric subpopulations, PA-2 and PB-1 (Figure 1C). PB-3 was associated with the fungal 164

parasite Cyttaria darwinii (14.29% of isolates, p-val = 0.039, F-statistic = 25.34 ) and 165

Nothofagus betuloides (28.57% of isolates, p-val = 5.02E-06, F-statistic = 60.35), which is only 166

found in southern Patagonia and is vicariant with N. dombeyi, a host of PB-1. PB-3 was 167

frequently isolated in southern Patagonia (49% of southern isolates) (Eizaguirre et al. 2018), and 168

its association with a southern-distributed tree species could play a role in its geographic range 169

and genetic isolation from the northern subpopulations. Neither Nothofagus nor A. araucana are 170

native to North America, and we found that our North American isolates were from multiple 171

diverse plant hosts, including Juniperus virginiana, Diospyros virginiana, Cedrus sp., and Pinus 172

sp. (Table S1), as well as from both soil and bark samples. In Patagonia, S. eubayanus has been 173

isolated from exotic Quercus trees (Eizaguirre et al. 2018), so even though Nothofagus and A. 174

araucana are common hosts, S. eubayanus can be found on a variety of hosts and substrates. 175

These observed differences in host and substrate could be playing a role in the maintenance of its 176

population structure, especially in sympatric regions of Patagonia. 177

178

All subpopulations grow at freezing temperatures and on diverse carbon sources: 179


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S. eubayanus comes from a wide range of environments, so we tested if there were 180

phenotypic differences between these subpopulations. We measured growth rates on several 181

carbon sources and stress responses for a large subset of these strains (190) and 26 lager-brewing 182

strains (Figure 2 and Figure S2). Lager-brewing strains grew faster on maltotriose than all 183

subpopulations (p-val < 0.05, Figure 2A), which is consistent with this sugar being one of the 184

most abundant in brewing wort but rare in nature (Salema-Oom et al. 2005). The Holarctic 185

subpopulation grew slower on glucose and maltose compared to all other subpopulations (p-val < 186

0.05, Figure 2A, Table S2). Overall, the admixed NoAm lineage performed better than PB-1 (p-187

val = 0.038, Figure 2A), but there was no interaction with carbon source. Therefore, the admixed 188

lineage’s robustness in many conditions could play a role in its success in far-flung North 189

American sites where no pure PA or PB strains have ever been found. 190

191 Figure 2. Phenotypic differences. 192 (A) Heat map of mean of maximum growth rate (change in OD/hour) (GR) on different carbon sources by 193 subpopulation. Warmer colors designate faster growth. (B) Heat map of log10 normalized growth at 194 different temperatures by subpopulation. 195 196

Since S. eubayanus’ contribution to the cold-adaptation of hybrid brewing strains is well 197

established (Libkind et al. 2011; Gibson et al. 2013; Baker et al. 2019), we measured growth at 198

0°C, 4°C, 10°C, and 20°C. All subpopulations grew at temperatures as low as 0°C (Figure 2B 199

GR

Raffinose

Maltotriose

Glycerol

EthanolGlucose

Maltose

Galactose

PA−2NoAmPA−1PB−2PB−3PB−1LagerHolarctic

0.01

0.02

0.03

0.04

0.05

0.06

RaffinoseMaltotriose

Glycerol

EthanolGlucose

Maltose

Galactose


0.01

0.02

0.03

0.04

0.05

0.06GR

20C10C0C 4C

LagerHolarcticPA−2NoAmPB−2PB−3PB−1PA−1 0.05

0.1

0.15

20C10C0C 4C


0.1

0.15BA


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and Figure S2), and all S. eubayanus subpopulations outperformed lager-brewing yeasts (p < 200

0.05). Within pure S. eubayanus, there were no temperature by subpopulation interactions, 201

indicating that no subpopulation is more cryotolerant than any other subpopulation. In summary, 202

we found that all strains that we tested grew similarly in many environments, and despite the 203

large amount of genotypic diversity observed for this species, we observed much less phenotypic 204

diversity (Figure 2). 205

206

Subpopulations are well differentiated: 207

The mating strategies and life cycle of Saccharomyces, with intratetrad mating and 208

haploselfing, often lead to homozygous diploid individuals (Hittinger 2013). Nonetheless, in S. 209

cerevisiae, many industrial strains are highly heterozygous (Gallone et al. 2016; Gonçalves et al. 210

2016; Peter et al. 2018). Here, we analyzed genome-wide heterozygosity in our collection of 200 211

strains and found only one individual with more than 20,000 heterozygous SNPs (Figure S3). 212

When we phased highly heterozygous regions of its genome and analyzed the two phases 213

separately, we found that both phases grouped within PB-1 (Figure S3C). Thus, while this strain 214

is highly heterozygous, it has contributions from only one subpopulation. 215

This large collection of strains is a powerful resource to explore natural variation and 216

population demography in a wild microbe, so we analyzed several common population genomic 217

statistics in 50-kbp windows across the genome. We found that diversity was similar between 218

subpopulations (Figure S4A). We also calculated Tajima’s D and found that the genome-wide 219

mean was zero or negative for each subpopulation (Figure S4B), which could be indicative of 220

population expansions. In particular, the most numerous and widespread subpopulation, PB-1, 221


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had the most negative and consistent Tajima’s D, suggesting a recent population expansion is 222

especially likely in this case. 223

224 Figure 3. Population genomic parameters. 225 (A) Network built with pairwise FST values < 0.8 between each subpopulation. FST values are printed and 226 correspond to line thickness, where lower values are thicker. Circle sizes correspond to genetic diversity. 227 (B) LD decay for each subpopulation (colors) and the species in whole (black). 228 229 For the non-admixed lineages, genome-wide average FST was consistently high across the 230

genome (Figure S4C). In pairwise comparisons of FST, PB-1 had the lowest values of any 231

subpopulation (Figure 3A, Figure S4D). These pairwise comparisons also showed that, within 232

each population, there has been some gene flow between subpopulations, even though the 233

subpopulations were generally well differentiated. Linkage disequilibrium (LD) decay indicated 234

low recombination in these wild subpopulations (Figure 3B), with variability between 235

subpopulations. For the species as a whole, LD decayed to one-half at about 5 kbp, which is 236

somewhat higher than the 500bp - 3kbp observed in S. cerevisiae (Liti et al. 2009; Schacherer et 237

al. 2009; Peter et al. 2018) and lower than the 9 kbp observed in S. paradoxus (Liti et al. 2009), 238

indicating that there is less mating, outcrossing, and/or recombination in this wild species than S. 239

cerevisiae and more than in S. paradoxus. 240

0.0

0.2

0.4

0.6

0KB 30KB 60KB 90KB 120KB 150KB 180KB 210KB 240KB 270KBSNP distance

r2

SubpopPA−1

PA−2

PB−1

PB−2

PB−3

Seub

A B

0.43

0.51

0.59

0.64

0.64

0.670.69

0.70

0.72

0.73

0.78

0.78

0.80

●

●

SoAm

NoAm

PA−1

PA−2

PB−1

PB−2

PB−3

Hol


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241

Recent admixture and historical gene flow between populations: 242

We previously reported the existence of 7 strains of an admixed lineage in Wisconsin, 243

USA, and New Brunswick, Canada (Peris et al. 2014, 2016). Here, we present 14 additional 244

isolates of this same admixed lineage. These new isolates were from the same site in Wisconsin, 245

as well as two new locations in North Carolina and South Carolina (Table S1). Strikingly, all 21 246

strains shared the exact same genome-wide ancestry profile (Figure 4A), indicating that they all 247

descended from the same outcrossing event between the two main populations of S. eubayanus. 248

These admixed strains were differentiated by 571 SNPs, which also delineated these strains 249

geographically (Figure 4B). Pairwise diversity and FST comparisons across the genomes suggest 250

that the PA parent came from the PA-2 subpopulation (Figure 4C and Figure S5A) and that the 251

PB parent was from the PB-1 subpopulation (Figure 4D and Figure S5A). 252

253 Figure 4. Genomic ancestries of NoAm and SoAm admixed lineages. 254

0.0

0.5

1.0

1.5

I II III IV VVI VII VIII IX X XI XII XIII XIV XV XVIGenome Position

Pairw

ise

Dive

rgen

ce (%

)

SubpopPB−1

PB−2

PB−3

0.0

0.5

1.0

1.5


Pairw

ise

Dive

rgen

ce (%

)

SubpopPA−1

PA−2

−5

0

5


log 2(d

A-So

Amd B

-SoA

m)

SoAmyHDPN421

yHDPN422

yHDPN423

yHDPN424

yHKB201

yHKB210

yHKB218

yHKB242

yHKB246

yHKB251

yHKB268

yHKS210

yHKS211

yHKS212

yHKS576

yHKS689

yHKS694

yHKS810

yHKS812

yHQL1481

yHQL1621

I II III IV VVIVIIVIII IX X XI XII XIIIXIVXVXVIGenome Position

log 2(d

A-N

oAm

d B-N

oAm)

0.0

0.5

1.0

1.5


Pairw

ise

Dive

rgen

ce (%

)

SubpopPB−1

PB−2

PB−3

0.0

0.5

1.0

1.5


Pairw

ise

Dive

rgen

ce (%

)

SubpopPA−1

PA−2

A

C

D

E

F

G

yHDPN421yHDPN424

yHDPN423

yHDPN422

yHKS211yHKS210

yHKS212

yHKS576yHKS689

yHKS694yHKB251

yHKB201yHQL1481

yHKS810yHQL1621yHKS812

yHKB210

yHKB218

yHKB246yHKB242

yHKB268

0.1

New Brunswick,

Canada South Carolina, USA

North Carolina, USAWisconsin,

USA

NoAm

B 0.1


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(A) For all 21 NoAm admixed strains, log2 ratio of the minimum PB-NoAm pairwise nucleotide sequence 255 divergence (dB-NoAm) and the minimum PA-NoAm pairwise nucleotide sequence divergence (dA-256 NoAm) in 50-kbp windows. Colors and log2 < 0 or > 0 indicate that part of the genome is more closely 257 related to PA or PB, respectively. (B) Neighbor-Net phylogenetic network reconstructed with the 571 258 SNPs that differentiate the NoAm strains. The scale bar represents the number of substitutions per site. 259 Collection location is noted. (C) Pairwise nucleotide sequence divergence of the NoAm strain yHKS210 260 compared to strains from the PA-1 and PA-2 subpopulations of PA in 50-kbp windows. (D) Pairwise 261 nucleotide sequence divergence of the NoAm strain yHKS210 compared to strains from the PB-1, PB-2, 262 and PB-3 subpopulations of PB in 50-kbp windows. (E) log2 ratio of the minimum PB-SoAm pairwise 263 nucleotide sequence divergence (dB-SoAm) and the minimum PA-SoAm pairwise nucleotide sequence 264 divergence (dA-SoAm) in 50-kbp windows. Colors and log2 < 0 or > 0 indicate that part of the genome is 265 more closely related to PA or PB, respectively. (F) Pairwise nucleotide sequence divergence of the SoAm 266 strain compared to strains from the PA-1 and PA-2 subpopulations of PA in 50-kbp windows. (G) 267 Pairwise nucleotide sequence divergence of the SoAm strain compared to strains of the PB-1, PB-2, and 268 PB-3 subpopulations of PB in 50-kbp windows. 269 270 Here, we report a second instance of recent outcrossing between PA and PB. One other 271

strain with fairly equal contributions from the two major populations, PA (~45%) and PB 272

(~55%) (Figure 4E), was isolated from the eastern side of Nahuel Huapi National Park, an area 273

that is sympatric for all subpopulations found in South America. This strain had a complex 274

ancestry, where both PA-1 and PA-2 contributed to the PA portions of its genome (Figure 4F and 275

Figure S5B), indicating that its PA parent was already admixed between PA-1 and PA-2. As with 276

the NoAm admixed strains, the PB parent was from the PB-1 subpopulation (Figure 4G and 277

Figure S5B). Together, these two admixed lineages show that outcrossing occurs between the 278

two major populations, and that admixture and gene flow are likely ongoing within sympatric 279

regions of South America. 280

We also found examples of smaller tracts of admixture between PA and PB that were 281

detectable as 2-12% contributions. These introgressed strains included the taxonomic type strain 282

of S. eubayanus (CBS12357T), whose genome sequence was mostly inferred to be from PB-1, 283

but it had a ~4% contribution from PA-1 (Figure S6). We found several other examples of 284

admixture between PA and PB, as well as admixture between subpopulations of PA or of PB 285

(Table S3). Notably, the PB contributions were usually from PB-1, the subpopulation with the 286


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largest range, most hosts, and strongest signature of population expansion, factors that would 287

tend to make contact with other subpopulations more likely. 288

In our collection of 200 strains, we observed nuclear genome contributions from S. 289

uvarum in four strains. These four strains all shared the same introgression of ~150-kbp on 290

chromosome XIV (Figure S7A&B). When we analyzed the portion of the genome contributed by 291

S. eubayanus, we found that these strains were all embedded in the PB-1 subpopulation (Figure 292

S7C). Analysis of the 150-kbp region from S. uvarum indicated that the closest S. uvarum 293

population related to these introgressed strains was SA-B (Figure S7D), a population restricted to 294

South America that has not previously been found to contribute to any known interspecies 295

hybrids (Almeida et al. 2014). These strains thus represent an independent hybridization event 296

between South American lineages of these two sister species that is not related to any known 297

hybridization events among industrial strains (Almeida et al. 2014). These strains show that S. 298

eubayanus and S. uvarum can and do hybridize in the wild, but the limited number (n=4) of 299

introgressed strains, small introgression size (150-kbp), and shared breakpoints suggest that the 300

persistence of hybrids in the wild is rare. 301

302

Northern Patagonia is a diversity hot spot: 303

Patagonia harbors the most genetic diversity of S. eubayanus in our dataset, and four 304

subpopulations were found only there: PA-1, PA-2, PB-2, and PB-3 (Figure 1A and 4A). 305

Therefore, we examined the genetic diversity and range distributions of the isolates from South 306

America more closely. Nahuel Huapi National Park yielded isolates from all five subpopulations 307

found in South America, was the only place where PA-1 was found, and was the location where 308

the SoAm admixed strain was isolated (Figure 5A & B). All five sub-populations were found 309


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north of 43°S, an important boundary during the last glaciation period that affects many 310

organisms (Mathiasen and Premoli 2010; Premoli et al. 2010; Quiroga and Premoli 2010). 311

Species-wide, there was more genetic diversity north of this boundary (Figure 5B). In contrast, 312

only PB-1 and PB-3 were found south of 43°S, with both distributions reaching Tierra del Fuego. 313

The southernmost strains were primarily PB-3 (89.7%), but they included two highly admixed 314

PB-1 × PB-3 strains (Table S1 & S3). 315

316 Figure 5. South American genomic diversity versus range, diversity by area, and isolation by distance. 317 (A) Range and genomic diversity of South American sampling sites. Circle sizes correspond to nucleotide 318 diversity of all strains from that site, and pie proportions correspond to each subpopulation’s contribution 319 to 𝜋 at each site. Latitudinal range of each subpopulation is shown to the right. (B) Nucleotide diversity 320 by subpopulation by sampling site, where larger and darker circles indicate more diversity. “SA Sites” in 321 gray show the diversity of all strains found in each South American (SA) site. “World Sites” in darker 322 gray show the nucleotide diversity of all North American or non-South American strains, regardless of 323 subpopulation, compared to South American strains south or north of 43°S, aligned to mean latitude of all 324 strains included in the analysis. (C) Correlation of nucleotide diversity and the area or distance a 325 subpopulation covers. The y-axis shows the nucleotide diversity of each subpopulation, and circle sizes 326 correspond to the geographic sizes of the subpopulations on a log10 scale. Note that PA-1 (dark red) is as 327 diverse as PB-3 (dark blue) but encompasses a smaller area. (D) log10(pairwise nucleotide diversity) 328 correlated with distance between strains, which demonstrates isolation by distance. Note that y-axes are 329 all scaled the same but not the x-axes. Holarctic includes the S. eubayanus sub-genome of two lager-330 brewing strains. Figure S8A shows the individual plots for the NoAm lineage. Figure S8B shows the 331 individual plot of PB-1. 332 333 Despite the limited geographic range of some subpopulations, their genetic diversity was 334

high, and this diversity often did not scale with the geographic area over which they were found 335

(Figure 5C). The widespread distribution of some subpopulations led us to question if there was 336

isolation by distance within a subpopulation (Figure 5D). We used pairwise measures of 337

−55

−50

−45

−40

PA−1 PA−2 PB−1 PB−2 PB−3 SoAm SASites

WorldSites

Latit

ude

NucleotideDiversity (%)

0.0

0.1

0.2

0.3

0.4

0.5

−55

−50

−45

−40

−75 −70 −65 −60Longitude

Latitude

PA−1 PA−2 PB−1 PB−2 PB−3

BA D

All North AmericanAll Non-South American

CPA−1 PA−2 NoAm PB−1 PB−2 PB−3 Hol

0 10 20 0 200 400 0 500 10001500 0 5000 10000 0 100 200 0 500 1000 1500 0 5000 10000

0.0001

0.0010

0.0100

0.1000

Distance (Km)

log(

Nuc

leot

ide

Dive

rsity

(%))

● ●

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●

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● ●

●

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● ●

0.00

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Area(10 Km^2)

Distance(Km)

Nuc

leot

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rsity

(%)

Subpopulation●●

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PA−1

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PB−1

PB−2

PB−3

NoAm

PopulationGeographicSize

100000

200000

300000

400000

p-val=0.0001 p-val=0.0001 p-val=0.0001 p-val=0.0001 p-val=0.0001p-val=0.0003p-val=0.564


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diversity and geographic distance between each strain and conducted Mantel tests for each 338

subpopulation. All subpopulations showed significant isolation by distance (Table S4), except 339

PA-1, likely because it had the smallest geographic range (25 km). Even the Mantel test for the 340

least diverse lineage, NoAm, was highly significant (p-val = 0.0001, R2= 0.106), indicating that 341

each location has been evolving independently after their recent shared outcrossing and dispersal 342

event. Through these pairwise analyses, we also detected two strains from Cerro Ñielol, Chile, 343

that were unusually genetically divergent from the rest of PB-1 and could potentially be a novel 344

lineage (Figure S8). 345

346

Additional global regions are climatically suitable: 347

The sparse but global distribution of S. eubayanus raises questions about whether other 348

areas of the world could be suitable for this species. We used the maxent environmental niche 349

modeling algorithm implemented in Wallace (Kass et al. 2018) to model the global climatic 350

suitability for S. eubayanus, using GPS coordinates of all known S. eubayanus strains published 351

here and estimates of coordinates for the East Asian isolates (Bing et al. 2014). These niche 352

models were built using the WorldClim Bioclims, which are based on monthly temperature and 353

rainfall measures, reflecting both annual and seasonal trends, as well as extremes, such as the 354

hottest and coldest quarters. How climatic variables affect yeast distributions is an understudied 355

area, and building these models allowed us a novel way to explore climatic suitability. 356

Using all known locations of isolation (Figure 6), we found that the best model 357

(AIC=2122.4) accurately delineated the known distribution along the Patagonian Andes. In 358

North America, the strains from the Olympic Mountains of Washington state and the Blue Ridge 359

region of North Carolina fell within the predicted areas, and interestingly, these sites had yielded 360


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pure PB-1 and Holarctic strains. In contrast, some of the NoAm admixed strains were found in 361

regions that were on the border of suitability in this model (New Brunswick and Wisconsin). In 362

Asia, the model predicts further suitable regions along the Himalayas that are west of known 363

locations. 364

365

Figure 6. Predicted climatic suitability of S. eubayanus. 366 Minimum training presence (light green) and 10th percentile training presence (dark green) based on a 367 model that includes all known S. eubayanus isolations, as well as a scenario of dispersal and 368 diversification out of Patagonia (inset and arrows). Black arrows signify diversification events, dotted 369 lines are diversification events where the population is not found in Patagonia, and colored arrows are 370 migration events for the lineage of matching color. Roman numerals order the potential migration events. 371 S. eubayanus has not been found in the wild in Europe, but it has contributed to fermentation hybrids, 372 such as lager yeasts. This scenario proposes that the last common ancestor of PA and PB-Holarctic 373 bifurcated into PA (red) and PB-Holarctic (blue), which further radiated into PA-1 (dark red), PA-2 (light 374 red), PB-1 (blue), PB-2 (lighter blue), PB-3 (dark blue), and Holarctic (very light blue). At least four 375 migration events are needed to explain the locations where S. eubayanus has been found. I. The Holarctic 376 subpopulation was drawn from the PB-Holarctic gene pool and colonized the Holarctic ecozone. II. PB-1 377 colonized the Pacific Rim, including New Zealand and Washington state, USA. III. An independent 378 dispersal event brought PB-1 to North Carolina, USA. IV. Outcrossing between PA-2 and PB-1 gave rise 379 to a low-diversity admixed linage that has recently invaded a large swath of North America. 380 381

The uneven global distribution of S. eubayanus led us to test if models were robust to 382

being built only with the South American locations or only with the non-South American 383

locations (Figure S9). Remarkably, with just the South American isolates, the model 384

(AIC=1327.32) accurately predicted the locations of the non-South American isolates (Figure 385

Predicted Climatic Suitability

Longitude

Latitude

40°S

20°S

0°

20°N

40°N

60°N

150°W 100°W 50°W 0° 50°E 100°E 150°E

0.0

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1.0

I

II

III

IV

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S9A). Even the model built from the limited number of isolates from outside South America 386

(AIC=558.58) still performed reasonably well, identifying the regions in Patagonia along the 387

Andes where S. eubayanus has been found (Figure S9B). Collectively, these models suggest that 388

climatic modeling can predict other suitable regions for eukaryotic microbes. These approaches 389

could be used to direct future sampling efforts or applied to other microbes to gain further insight 390

into microbial ecology. 391

Notably, all models agree that Europe is climatically a prime location for S. eubayanus 392

(Figure S9C), but no pure isolates have ever been found there, only hybrids with S. uvarum, S. 393

cerevisiae, or hybrids with even more parents (Almeida et al. 2014). These hybrids with complex 394

ancestries have been found in numerous fermentation environments, suggesting that pure S. 395

eubayanus once existed, or still exists at low abundance or in obscure locations, in Europe. Thus, 396

the lack of wild isolates from sampling efforts in Europe remains a complex puzzle. 397

398

Discussion: 399

Here, we integrated genomic, geographic, and phenotypic data for 200 strains of S. 400

eubayanus, the largest collection to date, to gain insight into its world-wide distribution, climatic 401

suitability, and population structure. All the strains belong to the two major populations 402

previously described (Peris et al. 2014, 2016), but with the extended dataset, we were able to 403

define considerable additional structure, consisting of six subpopulations and two admixed 404

lineages. These subpopulations have high genetic diversity, high FST, and long LD decay; all 405

measures indicative of large and partly isolated populations undergoing limited gene flow. 406

Despite this high genetic diversity, there was relatively little phenotypic differentiation between 407

subpopulations. This dichotomy between large genetic diversity and limited phenotypic 408


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differentiation hints at a complex demographic history where genetically differentiated 409

subpopulations are minimally phenotypically differentiated and grow well in a wide range of 410

environments. 411

Despite the strong population structure, we also observed considerable evidence of 412

admixture and gene flow. The two recently admixed lineages had nearly equal contributions 413

from the two major populations, but they were the result of independent outcrossing events. The 414

SoAm admixed strain was isolated from a hotspot of diversity and contains contributions from 415

three subpopulations. The NoAm admixed lineage has spread across at least four distant 416

locations, but all strains descended from the same outcrossing event. Since PA has only been 417

isolated in South America, it is intriguing that the NoAm admixed lineage has been successful in 418

so many locations throughout North America. The success of this lineage could be partially 419

explained by its equal or better performance in many environments in comparison to its parental 420

populations (Fig. 2), perhaps contributing to its invasion of several new locations. Several other 421

Patagonian strains also revealed more modest degrees of gene flow between PA and PB. Finally, 422

we characterized a shared nuclear introgression from S. uvarum into four Patagonian strains of S. 423

eubayanus, demonstrating that hybridization and backcrossing between these sister species has 424

occurred in the wild in South America. 425

S. eubayanus has a paradoxical biogeographical distribution; it is abundant in Patagonia, 426

but it is sparsely found elsewhere with far-flung isolates from North America, Asia, and Oceania. 427

Most subpopulations displayed isolation by distance, but genetic diversity only scaled with 428

geographic range to a limited extent. In Patagonia, some sampling sites harbor more genetic 429

diversity than all non-Patagonian locations together (Figure 5B). Although we found the most 430

genetic diversity and largest number of subpopulations north of 43°S, the pattern of genetic 431


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diversity appears to be reversed on the west side of the Andes, at least for the PB-1 432

subpopulation (Nespolo et al. 2019). This discrepancy could be due to differences in how glacial 433

refugia were distributed (Sérsic et al. 2011) and limitations on gene flow between the east and 434

west sides of the Andes. Together, the levels of S. eubayanus genetic diversity found within 435

Patagonia, as well as the restriction of four subpopulations to Patagonia, suggest that Patagonia is 436

the origin of most of the diversity of S. eubayanus, likely including the last common ancestor of 437

the PA and PB-Holarctic populations. 438

The simplest scenario to explain the current distribution and diversity of S. eubayanus is 439

a series of radiations in Patagonia, followed by a handful of out-of-Patagonia migration events 440

(Figure 6). Under this model, PA and PB would have bifurcated in Patagonia, possibly in 441

separate glacial refugia. The oldest migration event would have been the dispersal of the ancestor 442

of the Holarctic subpopulation, drawn from the PB gene pool, to the Northern Hemisphere. 443

Multiple more recent migration events could have resulted in the few PB-1 strains found in New 444

Zealand and the USA. The New Zealand and Washington state strains cluster phylogenetically 445

and could have diversified from the same migration event from Patagonia into the Pacific Rim. 446

The PB-1 strain from North Carolina (yHKB35) is genetically more similar to PB-1 strains from 447

Patagonia, suggesting it arrived in the Northern Hemisphere independently of the Pacific Rim 448

strains. Finally, the NoAm admixed strains are likely the descendants of a single, and relatively 449

recent, out-of-Patagonia dispersal. Given that PA appears to be restricted to northern Patagonia, 450

this region could have been where the hybridization leading to the NoAm lineage occurred. 451

While the dispersal vector that brought this admixed lineage to North America is unknown, its 452

far-flung distribution and low diversity show that it has rapidly succeeded by invading new 453

environments. 454


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Other more complex scenarios could conceivably explain the limited number of strains 455

found outside of Patagonia. For example, PA and PB could represent sequential colonizations of 456

Patagonia from the Northern Hemisphere. Under this model, PA would have arrived first and 457

would then have been restricted to northern Patagonia by competition with the later arrival of 458

PB. The Holarctic subpopulation could be interpreted as remnants of the PB population that did 459

not migrate to Patagonia; but the PB-1 strains from the Northern Hemisphere, especially 460

yHKB35, seem far more likely to have been drawn from a Patagonian gene pool than the other 461

way around. Furthermore, the structuring of the PA-1 and the PA-2 subpopulations and of the 462

PB-1, PB-2, and PB-3 subpopulations are particularly challenging to rectify with models that do 463

not allow for diversification within South America. Even more complex scenarios remain 464

possible, and more sampling and isolation will be required to fully elucidate the distribution of 465

this elusive species and more conclusively reject potential biogeographical models. 466

S. eubayanus has a strikingly parallel population structure and genetic diversity to its 467

sister species S. uvarum (Almeida et al. 2014; Peris et al. 2016). Both species are abundant and 468

diverse in Patagonia but can be found globally. Both have early diverging lineages, found in Asia 469

or Australasia, that border on being considered novel species. In South America, both have two 470

major populations, where one of these populations is restricted to northern Patagonia (north of 471

43°S). However, a major difference between the distribution of these species is that pure strains 472

of S. uvarum have been found in Europe. Many dimensions of biodiversity could be interacting 473

to bound the distribution and population structure of both S. eubayanus and S. uvarum. In 474

particular, we know very little about local ecology, including the biotic community and 475

availability of abiotic resources on a microbial scale, but these factors likely all influence 476

microbial success. We show here that substrate and host association vary between 477


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subpopulations. In Patagonia, S. eubayanus and S. uvarum are commonly associated with 478

Nothofagus, where N. dombeyi is the preferred host of S. uvarum (Libkind et al. 2011; Eizaguirre 479

et al. 2018). Therefore, niche partitioning of host trees could be playing role in the persistence of 480

these species in sympatry in Patagonia. However, in locations where Nothofagus is not found and 481

there are perhaps fewer hosts, competitive exclusion between the sister species S. eubayanus and 482

S. uvarum, could influence distribution. Competition for a narrower set of hosts could potentially 483

explain why only S. uvarum has been found in Europe as pure strains, while S. eubayanus has 484

not. A second factor influencing distribution and population structure could be dispersal. Yeasts 485

could migrate via many avenues, such as wind, insect, bird, or other animals (Francesca et al. 486

2012, 2014; Stefanini et al. 2012; Gillespie et al. 2012). Human mediated-dispersal has been 487

inferred for the S. cerevisiae Wine and Beer lineages and for the S. paradoxus European/SpA 488

lineage (Gallone et al. 2016; Gonçalves et al. 2016; Leducq et al. 2014; Kuehne et al. 2007). A 489

third bounding factor could be a region’s historical climate. Glacial refugia act as reservoirs of 490

isolated genetic diversity that allow expansion into new areas after glacial retreat (Stewart and 491

Lister 2001). 43°S is a significant geographic boundary due to past geological and climatic 492

variables (Mathiasen and Premoli 2010; Eizaguirre et al. 2018), and many other species and 493

genera show a distinction between their northern and southern counterparts, including 494

Nothofagus (Mathiasen and Premoli 2010; Premoli et al. 2012). S. eubayanus and S. uvarum 495

diversities are also strongly affected by the 43°S boundary (Almeida et al. 2014; Eizaguirre et al. 496

2018), and it seems likely that the microbes experienced some of the same glaciation effects as 497

their hosts. The strong correlation of S. eubayanus and S. uvarum population structures with 498

43°S further implies a longstanding and intimate association with Patagonia. 499


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The sparse global distribution and complex patterns of genetic diversity continue to raise 500

questions about the niche and potential range of S. eubayanus. Our climatic modeling suggests 501

that parts of Europe would be ideal for S. eubayanus. Despite extensive sampling efforts, S. 502

eubayanus has never been isolated in Europe (Sampaio 2018). However, recent environmental 503

sequencing of the fungal specific ITS1 region hinted that S. eubayanus may exist in the wild in 504

Europe (Alsammar et al. 2019). Considerable caution is warranted in interpreting this result 505

because the rDNA locus quickly fixes to one parent’s allele in interspecies hybrids, there is only 506

a single ITS1 SNP between S. uvarum and S. eubayanus, and the dataset contained very few 507

reads that mapped to S. eubayanus. Still, the prevalence of hybrids with contributions from the 508

Holarctic lineage of S. eubayanus found in Europe (Peris et al. 2016) suggests that the Holarctic 509

lineage exists in Europe, or at least existed historically, allowing it to contribute to many 510

independent hybridization events. 511

The patterns of radiation and dispersal observed here mirror the dynamics of evolution 512

found in other organisms (Czekanski-Moir and Rundell 2019), including humans (Nielsen et al. 513

2017). S. eubayanus and humans harbor diverse and structured populations in sub-Saharan 514

Africa and Patagonia, respectively. In these endemic regions, both species show signals of 515

ancient and recent admixture between these structured populations. Both species have 516

successfully colonized wide swaths of the globe, with the consequence of repeated bottlenecks in 517

genetic diversity. While anatomically modern humans underwent a single major out-of-Africa 518

migration that led to the peopling of the world (Nielsen et al. 2017), S. eubayanus has 519

experienced several migration events from different populations that have led to more punctate 520

global distribution. For both species, intraspecific admixture and interspecific hybridization 521

appear to have played adaptive roles in the success of colonizing these new locations. In humans, 522


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introgressions from past hybridizations with both Neanderthals and Denisovans underlie many 523

adaptive traits (Racimo et al. 2015), while the cold fermentation of lager-brewing would not be 524

possible without the cryotolerance of S. eubayanus and the aggressive fermentation of 525

domesticated ale strains of S. cerevisiae (Gibson and Liti 2015). These parallels illustrate how 526

the biogeographical and evolutionary dynamics observed in plants and animals also shape 527

microbial diversity. As yeast ecology and population genomics (Marsit et al. 2017; Yurkov 528

2017) move beyond the Baas-Becking “Everything is everywhere” hypothesis of microbial 529

ecology (Baas-Becking 1934; de Wit and Bouvier 2006), the rich dynamics of natural diversity 530

that is hidden in the soil at our feet is being uncovered. 531

532

Methods: 533

Wild strain isolations 534

All South American isolates were sampled, isolated, and identified as described 535

previously (Libkind et al. 2011; Eizaguirre et al. 2018). North American isolates new to this 536

publication were from soil or bark samples from the American states of Washington, Wisconsin, 537

North Carolina, and South Carolina (Table S1). Strain enrichment and isolation was done as 538

previously described (Sylvester et al. 2015; Peris et al. 2016, 2014), with a few exceptions in 539

temperature and carbon source of isolation (Table S1). Specifically, two strains were isolated at 540

4°C, eight strains were isolated at room temperature, and six strains were isolated on a non-541

glucose carbon source: three in galactose, two in sucrose, and one in maltose (Table S1). 542

543

Whole genome sequencing and SNP-calling 544


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Whole genome sequencing was completed with Illumina paired-end reads as described 545

previously (Peris et al. 2016; Shen et al. 2018). Reads were aligned to the reference genome 546

(Baker et al. 2015), SNPs were called, masked for low coverage, and retained for downstream 547

analysis as described previously (Peris et al. 2016). One strain, yHCT75, had more than 20,000 548

heterozygous SNPs called. This strain was pseudo-phased using read-backed phasing in GATK 549

(McKenna et al. 2010) and split into two phases. Short-read data is deposited in the NCBI Short 550

Read Archive under PRJNA555221. 551

552

Population genomic analyses: 553

Population structure was defined using several approaches: fastSTRUCTURE (Raj et al. 554

2014), fineSTRUCTURE (Lawson et al. 2012), SplitsTree v4 (Huson and Bryant 2006), 555

and Principal Component Analysis with the adegenet package in R (Jombart 2008). 556

fineSTRUCTURE analysis was completed using all strains and 11994 SNPs. The 557

SplitsTree network was built with this same set of strains and SNPs. fastStructure 558

analysis was completed with as subsample of 5 NoAm strains and 150165 SNPs. We tested K=1 559

through K=10 and selected K=6 using the “chooseK.py” command in fastSTRUCTURE. All 560

calculations of pairwise divergence, FST, and Tajima’s D for subpopulations were computed 561

using the R package PopGenome (Pfeifer and Wittelsbuerger 2015) in windows of 50-kbp. 562

Pairwise divergence between strains was calculated across the whole genome using PopGenome. 563

LD was calculated using PopLDdecay (Zhang et al. 2019). Geographic area and distance of 564

subpopulations was calculated using the geosphere package in R (Hijmans et al. 2019). The 565

Mantel tests were completed using ade4 package of R (Dray and Dufour 2007). The FST network 566

was built with iGraph in R (Csardi and Nepusz 2006). 567


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26

568

Niche projection with Wallace: 569

Climatic modeling of S. eubayanus was completed using the R package Wallace (Kass et 570

al. 2018). Three sets of occurrence data were tested: one that included only GPS coordinates for 571

strains from South America, one that included only non-South American isolates, and one that 572

included all known isolates (Table S1). We could use exact GPS coordinates for most strains, 573

except for the strains from East Asia, where we estimated the locations (Bing et al. 2014). 574

WorldClim bioclimatic variables were obtained at a resolution of 2.5 arcmin. The background 575

extent was set to “Minimum convex polygon” with a 0.5-degree buffer distance and 10,000 576

background points were sampled. We used block spatial partitioning. The model was built using 577

the Maxent algorithm, using the feature classes: L (linear), LQ (linear quadradic), H (Hinge), 578

LQH, and LQHP (Linear Quadradic Hinge Product) with 1-3 regularization multipliers and the 579

multiplier step value set to 1. The model was chosen based on the Akaike Information Criterion 580

(AIC) score (Table S5). The best models were then projected to the all continents, except 581

Antarctica. 582

583

Phenotyping: 584

Strains were first revived in Yeast Peptone Dextrose (YPD) and grown for 3 days at room 585

temperature. These saturated cultures were then transferred to two 96-well microtiter plates, for 586

growth rate and stress tolerance phenotyping. These plates were incubated overnight. Cells were 587

pinned from these plates into plates for growth rate measurements. For temperature growth 588

assays, cells were pinned into four fresh YPD microtiter plates and then incubated at 0°C, 4°C, 589

10°C, and 20°C. For the microtiter plates at 0°C, 4°C, and 10°C, OD was measured at least once 590


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27

a day for two weeks or until a majority of the strains had reached stationary phase. Growth on 591

different carbon sources was measured at 20°C in MM media with 2% of the respective carbon 592

source. Carbon sources tested were: glucose, galactose, raffinose, maltose, maltotriose, ethanol, 593

and glycerol. OD was read every two hours for one week or until saturation. All phenotyping 594

was completed in biological triplicate. The carbon source data was truncated to 125 hours to 595

remove artifacts due to evaporation. Growth curves were analyzed using the package grofit 596

(Kahm et al. 2010) in R to measure saturation and growth rate. We then averaged each strain 597

over the triplicates. We used an ANOVA corrected with Tukey’s HSD to test for growth rate 598

interactions between subpopulation and carbon source or subpopulation and temperature. We 599

used the R package pvclust (Suzuki and Shimodaira 2006) to cluster and build heatmaps of 600

growth rate by subpopulation. 601

Heat shock was completed by pelleting 200μl saturated culture, removing supernatant, 602

resuspending in 200μl YPD pre-heated to 37°C, and incubating for one hour at 37°C, with a 603

room temperature control. Freeze-thaw tolerance was tested by placing saturated YPD cultures in 604

a dry ice ethanol bath for two hours, with a control that was incubated on ice. After stress, the 605

strains were serially diluted 1:10 three times and pinned onto solid YPD. These dilution plates 606

were then photographed after 6 and 18 hours. CellProfiler (Lamprecht et al. 2007) was 607

used to calculate the colony sizes after 18 hours, and the 3rd (1:1000) dilutions were used for 608

downstream analyses. The heat shock measurements were normalized by the room temperature 609

controls, and the freeze thaw measurements were normalized by the ice incubation controls. 610

Statistical interactions of subpopulations and stress responses were tested as above. 611

612

Data Availability: 613


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All short-read genome sequencing data has been deposited in the NCBI Short Read Archive 614

under the PRJNA555221. Accessions of public data is given in Table S1. 615

616

Acknowledgements: 617

We thank Francisco A. Cubillos for coordinating publication with their study; Sean D. Schoville, 618

José Paulo Sampaio, Paula Gonçalves, and members of the Hittinger Lab, in particular 619

EmilyClare P. Baker, for helpful discussion and feedback; Amanda B. Hulfachor and Martin 620

Bontrager for preparing a subset of Illumina libraries; the University of Wisconsin 621

Biotechnology Center DNA Sequencing Facility for providing Illumina sequencing facilities and 622

services; the Agricultural Research Service (ARS) NRRL collection, Christian R. Landry, 623

Ashley Kinart, and Drew T. Doering for strains included in phenotyping; Huu-Vang Nguyen for 624

strains used for hybrid genome comparison; and Leslie Shown, Anita R. & S. Todd Hittinger, 625

EmilyClare P. Baker, and Ryan V. Moriarty for collecting samples and/or isolating strains. This 626

material is based upon work supported by the National Science Foundation under Grant Nos. 627

DEB-1253634 (to CTH) and DGE-1256259 (Graduate Research Fellowship to QKL), the USDA 628

National Institute of Food and Agriculture Hatch Project No. 1003258 to CTH, and in part by the 629

DOE Great Lakes Bioenergy Research Center (DOE BER Office of Science Nos. DE-630

SC0018409 and DE-FC02-07ER64494 to Timothy J. Donohue). QKL was also supported by the 631

Predoctoral Training Program in Genetics, funded by the National Institutes of Health 632

(5T32GM007133). DP is a Marie Sklodowska-Curie fellow of the European Union’s Horizon 633

2020 research and innovation program (Grant Agreement No. 747775). DL was supported by 634

CONICET (PIP11220130100392CO), FONCyT (PICT 3677, PICT 2542), Universidad Nacional 635

del Comahue (B199), and NSF-CONICET grant. CTH is a Pew Scholar in the Biomedical 636


https://doi.org/10.1101/709535


29

Sciences and H. I. Romnes Faculty Fellow, supported by the Pew Charitable Trusts and Office of 637

the Vice Chancellor for Research and Graduate Education with funding from the Wisconsin 638

Alumni Research Foundation (WARF), respectively. 639

640

Author Contributions: 641

QKL, DL, and CTH, conceived of the study; QLK, DP, JIE, DL, and CTH refined concept and 642

design; QKL performed all population genomic and ecological niche analyses; QKL and DAO 643

sequenced genomes, performed phenotyping and statistical analyses, and mentored KVB and 644

MJ; DL and CTH supervised the study; KVB, KS, and MJ isolated and/or identified North 645

American strains; JIE, MER, CAL, and DL isolated and/or provided South American strains; and 646

QKL and CTH wrote the manuscript with editorial input from all co-authors. 647

648

Conflict of Interest Disclosure: 649

Commercial use of Saccharomyces eubayanus strains requires a license from WARF or 650

CONICET. Strains are available for academic research under a material transfer agreement. 651

652

References: 653

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Alsammar HF, Naseeb S, Brancia LB, Gilman RT, Wang P, Delneri D. 2019. Targeted 657 metagenomics approach to capture the biodiversity of Saccharomyces genus in wild 658 environments. Environ Microbiol Rep 11: 206–214. 659

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Baker EP, Peris D, Moriarty R V, Li XC, Fay JC, Hittinger CT. 2019. Mitochondrial DNA and 665 temperature tolerance in lager yeasts. Sci Adv 5: eaav1869. 666


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817 Figure Legends: 818

Figure 1. S. eubayanus distribution and population structure. 819

S. eubayanus has a global distribution and two major populations with six subpopulations. (A) 820

Isolation locations of S. eubayanus strains included in the dataset. For visibility, circle size is not 821

scaled by the number of strains. Subpopulation abundance is shown as pie charts. The 822

Patagonian sampling sites have been collapsed to two locations for clarity. Details of sites and 823

subpopulations found in South America (B) and North America (C) with circle size scaled by the 824

number of strains. (D) Whole genome PCA of S. eubayanus strains and five hybrids with large 825

contributions from S. eubayanus. (E) PCA of just PA. (F) PCA of just PB and hybrid S. 826

eubayanus sub-genomes. Color legends in A and D apply to this and all other figures. 827

828

Figure 2. Phenotypic differences. 829

(A) Heat map of mean of maximum growth rate (change in OD/hour) (GR) on different carbon 830

sources by subpopulation. Warmer colors designate faster growth. (B) Heat map of log10 831

normalized growth at different temperatures by subpopulation. 832

833

Figure 3. Population genomic parameters. 834

(A) Network built with pairwise FST values < 0.8 between each subpopulation. FST values are 835

printed and correspond to line thickness, where lower values are thicker. Circle sizes correspond 836

to genetic diversity. (B) LD decay for each subpopulation (colors) and the species in whole 837

(black). 838

839


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34

Figure 4. Genomic ancestries of NoAm and SoAm admixed lineages. 840

(A) For all 21 NoAm admixed strains, log2 ratio of the minimum PB-NoAm pairwise nucleotide 841

sequence divergence (dB-NoAm) and the minimum PA-NoAm pairwise nucleotide sequence 842

divergence (dA-NoAm) in 50-kbp windows. Colors and log2 < 0 or > 0 indicate that part of the 843

genome is more closely related to PA or PB, respectively. (B) Neighbor-Net phylogenetic 844

network reconstructed with the 571 SNPs that differentiate the NoAm strains. The scale bar 845

represents the number of substitutions per site. Collection location is noted. (C) Pairwise 846

nucleotide sequence divergence of the NoAm strain yHKS210 compared to strains from the PA-847

1 and PA-2 subpopulations of PA in 50-kbp windows. (D) Pairwise nucleotide sequence 848

divergence of the NoAm strain yHKS210 compared to strains from the PB-1, PB-2, and PB-3 849

subpopulations of PB in 50-kbp windows. (E) log2 ratio of the minimum PB-SoAm pairwise 850

nucleotide sequence divergence (dB-SoAm) and the minimum PA-SoAm pairwise nucleotide 851

sequence divergence (dA-SoAm) in 50-kbp windows. Colors and log2 < 0 or > 0 indicate that 852

part of the genome is more closely related to PA or PB, respectively. (F) Pairwise nucleotide 853

sequence divergence of the SoAm strain compared to strains from the PA-1 and PA-2 854

subpopulations of PA in 50-kbp windows. (G) Pairwise nucleotide sequence divergence of the 855

SoAm strain compared to strains of the PB-1, PB-2, and PB-3 subpopulations of PB in 50-kbp 856

windows. 857

858

Figure 5. South American genomic diversity versus range, diversity by area, and isolation by 859

distance. 860

(A) Range and genomic diversity of South American sampling sites. Circle sizes correspond to 861

nucleotide diversity of all strains from that site, and pie proportions correspond to each 862

subpopulation’s contribution to 𝜋 at each site. Latitudinal range of each subpopulation is shown 863

to the right. (B) Nucleotide diversity by subpopulation by sampling site, where larger and darker 864

circles indicate more diversity. “SA Sites” in gray show the diversity of all strains found in each 865

South American (SA) site. “World Sites” in darker gray show the nucleotide diversity of all 866

North American or non-South American strains, regardless of subpopulation, compared to South 867

American strains south or north of 43°S, aligned to mean latitude of all strains included in the 868

analysis. (C) Correlation of nucleotide diversity and the area or distance a subpopulation covers. 869

The y-axis shows the nucleotide diversity of each subpopulation, and circle sizes correspond to 870


https://doi.org/10.1101/709535


35

the geographic sizes of the subpopulations on a log10 scale. Note that PA-1 (dark red) is as 871

diverse as PB-3 (dark blue) but encompasses a smaller area. (D) log10(pairwise nucleotide 872

diversity) correlated with distance between strains, which demonstrates isolation by distance. 873

Note that y-axes are all scaled the same but not the x-axes. Holarctic includes the S. eubayanus 874

sub-genome of two lager-brewing strains. Figure S8A shows the individual plots for the NoAm 875

lineage. Figure S8B shows the individual plot of PB-1. 876

877

Figure 6. Predicted climatic suitability of S. eubayanus. 878

Minimum training presence (light green) and 10th percentile training presence (dark green) based 879

on a model that includes all known S. eubayanus isolations, as well as a scenario of dispersal and 880

diversification out of Patagonia (inset and arrows). Black arrows signify diversification events, 881

dotted lines are diversification events where the population is not found in Patagonia, and 882

colored arrows are migration events for the lineage of matching color. Roman numerals order the 883

potential migration events. S. eubayanus has not been found in the wild in Europe, but it has 884

contributed to fermentation hybrids, such as lager yeasts. This scenario proposes that the last 885

common ancestor of PA and PB-Holarctic bifurcated into PA (red) and PB-Holarctic (blue), 886

which further radiated into PA-1 (dark red), PA-2 (light red), PB-1 (blue), PB-2 (lighter blue), 887

PB-3 (dark blue), and Holarctic (very light blue). At least four migration events are needed to 888

explain the locations where S. eubayanus has been found. I. The Holarctic subpopulation was 889

drawn from the PB-Holarctic gene pool and colonized the Holarctic ecozone. II. PB-1 colonized 890

the Pacific Rim, including New Zealand and Washington state, USA. III. An independent 891

dispersal event brought PB-1 to North Carolina, USA. IV. Outcrossing between PA-2 and PB-1 892

gave rise to a low-diversity admixed linage that has recently invaded a large swath of North 893

America. 894

895

Supplementary Figure 1. Additional visualizations of population structure. 896

(A) SplitsTree network tree built with 11994 SNPs with subpopulations circled and labeled. (B) 897

FineStructure co-ancestry plot built with 11994 SNPs. Bluer colors correspond to more genetic 898

similarity. Boxes have been added to label the subpopulations. (C) FastSTRUCTURE plot (K=6) 899

built with 150165 SNPs and showing the same six monophyletic subpopulations found with 900

other approaches. Only five NoAm strains were included in the fastSTRUCTURE analysis. 901


https://doi.org/10.1101/709535


36

902

Supplementary Figure. 2. Additional phenotypic data. 903

(A) Violin plots of recovery from stress, normalized by controls. There were no significant 904

subpopulation by stress interactions. (B) Violin plots of log10 normalized mean growth rates of 905

each subpopulation at 0°C, 4°C, 10°C, and 20°C. * = p-val < 0.05 of interactions between Lager 906

and PA-2, PB-2, and PB-3 at 10°C; Lager and PA-1, PA-2, PB-1, PB-2, and PB-3 at 20°C; and 907

PB-2 and both PA-2 and NoAm at 20°C (C) Violin plots of mean growth rate on different carbon 908

sources (* = p-val < 0.05). (D) Heatmaps of significant subpopulation by temperature 909

interactions and (E) significant subpopulation by carbon source interactions. Warmer colors 910

indicate that the subpopulation-temperature or carbon source on the left hand had a faster growth 911

rate than the subpopulation-temperature or carbon source along the bottom; cooler colors 912

represent the reverse. Non-significant interactions, based on multiple test corrections, are in 913

white. More intense colors represent smaller p-values. 914

915

Supplementary Figure 3. Heterozygosity analyses. 916

(A) Summary of all SNPs vs SNPs called as heterozygous compared to the taxonomic type strain 917

for all 200 strains included in this study. The upper limit of the bar is the total SNP count. The 918

lower point corresponds to SNPs called as heterozygous. The horizontal line is 20k SNPs. (B) 919

Strain yHCT75 (CRUB 1946) is the only strain with > 20K heterozygous SNPs. (C) When the 920

heterozygous SNPs of yHCT75 were pseudo-phased (labeled), both phases clustered with PB-1. 921

922

Supplementary Figure 4. Additional population genomic statistics. 923

(A) Mean pairwise nucleotide diversity (𝜋 * 100) for each subpopulation across the genome in 924

50-kbp windows. (B) Tajima’s D across the genome in 50-kbp windows for each subpopulation. 925

(C) Mean FST in 50-kpb windows for each subpopulation compared to all subpopulations. (D) 926

Pairwise FST for each subpopulation compared to PB-1. 927

928

Supplementary Figure 5. Pairwise FST plots for NoAm and SoAm compared to all other 929

subpopulations. 930

Pairwise FST for the NoAm lineage (A) or SoAm strain (B) compared to all other subpopulations. 931

932


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Supplementary Figure 6. The taxonomic type strain has a mosaic genome. 933

(A) Pairwise genetic divergence of the taxonomic type strain compared to each subpopulation. 934

(B) Comparison of pairwise genetic divergence of the taxonomic type strain compared to PA-1 935

and PB-1. (C) log2 divergence plot (as in Figure 4) showing regions introgressed from PA-1 in 936

the taxonomic type strain. 937

938

Supplementary Figure 7. Four S. eubayanus strains with S. uvarum nuclear introgressions. 939

(A) Depth of coverage plots of reads from four strains mapped to both the S. uvarum (Suva) and 940

S. eubayanus (Seub) reference genomes. (B) Zoom-in of region on Chromosome XIV where 941

these four strains have the same S. uvarum (purple) introgression into a S. eubayanus 942

background. (C) A PCA plot shows that these four strains belong to the PB-1 subpopulation of S. 943

eubayanus. (D) A PCA plot shows that the introgressed region from S. uvarum came from the 944

South American SA-B subpopulation of S. uvarum. 945

946

Supplementary Figure 8. Isolation by distance plots for NoAm and PB-1. 947

(A) Isolation by distance for all NoAm strains. The y-axis has been rescaled compared to Figure 948

5 for better visualization. (B) Isolation by distance for subpopulation PB-1. Comparisons with 949

strains from Cerro Ñielol are labeled. All comparisons of South American strains with non-South 950

American strains are on the right side. 951

952

Supplementary Figure 9. Additional Wallace climatic models. 953

(A) Model built using only South American isolation locations. (B) Model built using only non-954

South American sites. (C) Comparison of models based on all known S. eubayanus collection 955

sites, only South American, or only non-South American sites. Where the models agree is in dark 956

green, where two models agree is in medium green, and where one model predicts suitability is 957

in light green. 958

959

Supplementary Table 1. Collection information for all strains whose genomes were sequenced or 960

analyzed in this study. 961

962


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Supplementary Table 2. Average triplicate growth rates for various temperatures and carbon 963

sources. Note that this spreadsheet has multiple sheets. 964

965

Supplementary Table 3. K=6 output of FastSTRUCTURE. 966

967

Supplementary Table 4. Mantel test results. 968

969

Supplementary Table 5. Input and output for Wallace climatic modeling. 970


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25

30

35

40

45

50

−120 −100 −80 −60Longitude

Latitude

PB−1

PB−2

PB−3Holarctic

PA−1 PA−2

NoAm

SoAm

−150

−100

−50

0

50

−100 0 100 200PC1 = 40.06%

PC2

= 9.

95%

PA−1

PA−2

PB−1

PB−2

PB−3

Holarctic

Hybrid

NoAm

SoAm

PA−1PA−2

−75

−50

−25

0

25

50

−150 −100 −50 0 50PC1 = 41.56%

PC2

= 7.

81%

PA−1

PA−2

−50

0

50

−100 0 100 200Longitude

Latitude

PA−1PA−2

PB−1PB−2

PB−3Holarctic

NoAmSoAm

Figure 1

−55

−50

−45

−40

−75 −70 −65 −60Longitude

Latitude

B

C

E

D

A

PB1

PB−2

PB−3

Holarctic−50

0

50

−50 0 50 100PC1 = 19.03%

PC2

= 13

.96%

PB−1

PB−2

PB−3

Holarctic

Hybrid

F


https://doi.org/10.1101/709535


Figure 2

0.0

0.2

0.4

0.6

0KB 30KB 60KB 90KB 120KB 150KB 180KB 210KB 240KB 270KBSNP distance

r2Subpop

PA−1

PA−2

PB−1

PB−2

PB−3

Seub

A B

GR

Raffinose

Maltotriose

Glycerol

EthanolGlucose

Maltose

Galactose


0.01

0.02

0.03

0.04

0.05

0.06

Raffinose

Maltotriose

Glycerol

EthanolGlucose

Maltose

Galactose


0.01

0.02

0.03

0.04

0.05

0.06GR

20C10C0C 4C


0.1

0.15

20C10C0C 4C


0.1

0.15BA

20C10C0C 4C


0.1

0.15

20C10C0C 4C


0.1

0.15

Figure 3

0.43

0.51

0.59

0.64

0.64

0.670.69

0.70

0.72

0.73

0.78

0.78

0.80

●

●

SoAm

NoAm

PA−1

PA−2

PB−1

PB−2

PB−3

Hol


https://doi.org/10.1101/709535


0.0

0.5

1.0

1.5


Pairw

ise

Dive

rgen

ce (%

)

SubpopPB−1

PB−2

PB−3

0.0

0.5

1.0

1.5


Pairw

ise

Dive

rgen

ce (%

)

SubpopPA−1

PA−2

−5

0

5


log 2(d

A-So

Amd B

-SoA

m)

SoAmyHDPN421

yHDPN422

yHDPN423

yHDPN424

yHKB201

yHKB210

yHKB218

yHKB242

yHKB246

yHKB251

yHKB268

yHKS210

yHKS211

yHKS212

yHKS576

yHKS689

yHKS694

yHKS810

yHKS812

yHQL1481

yHQL1621

I II III IV VVIVIIVIII IX X XI XII XIIIXIVXVXVIGenome Position

log 2(d

A-N

oAm

d B-N

oAm)

0.0

0.5

1.0

1.5


Pairw

ise

Dive

rgen

ce (%

)

SubpopPB−1

PB−2

PB−3

0.0

0.5

1.0

1.5


Pairw

ise

Dive

rgen

ce (%

)

SubpopPA−1

PA−2

Figure 4 A

C

D

E

F

G

yHDPN421yHDPN424

yHDPN423

yHDPN422

yHKS211yHKS210

yHKS212

yHKS576yHKS689

yHKS694yHKB251

yHKB201yHQL1481

yHKS810yHQL1621yHKS812

yHKB210

yHKB218

yHKB246yHKB242

yHKB268

0.1

New Brunswick,

Canada South Carolina, USA

North Carolina, USAWisconsin,

USA

NoAm

B 0.1


https://doi.org/10.1101/709535


−55

−50

−45

−40

PA−1 PA−2 PB−1 PB−2 PB−3 SoAm SASites

WorldSites

Latit

ude

NucleotideDiversity (%)

0.0

0.1

0.2

0.3

0.4

0.5

−55

−50

−45

−40

−75 −70 −65 −60Longitude

Latitude

PA−1 PA−2 PB−1 PB−2 PB−3

Figure 5BA D

All North AmericanAll Non-South American

CPA−1 PA−2 NoAm PB−1 PB−2 PB−3 Hol

0 10 20 0 200 400 0 500 10001500 0 5000 10000 0 100 200 0 500 1000 1500 0 5000 10000

0.0001

0.0010

0.0100

0.1000

Distance (Km)

log(

Nuc

leot

ide

Dive

rsity

(%))

● ●

● ●

●

● ●

● ●

●

● ●

● ●

0.00

0.05

0.10

0.15

0.20

Area(10 Km^2)

Distance(Km)

Nuc

leot

ide

Dive

rsity

(%)

Subpopulation●●

●●

●●

●●

●●

●●

PA−1

PA−2

PB−1

PB−2

PB−3

NoAm

PopulationGeographicSize

100000

200000

300000

400000

p-val=0.0001 p-val=0.0001 p-val=0.0001 p-val=0.0001 p-val=0.0001p-val=0.0003p-val=0.564


https://doi.org/10.1101/709535


Figure 6

Predicted Climatic Suitability

Longitude

Latitude

40°S

20°S

0°

20°N

40°N

60°N

150°W 100°W 50°W 0° 50°E 100°E 150°E

0.0

0.5

1.0

I

II

III

IV

Ancestor


https://doi.org/10.1101/709535


Figure S1

PB -3

PB -2

Holarctic

PA -2

PA -1

NoAm

SoAm

PB -1

B

A

Holarctic PB -2 PA -2 PA -1 PB -3 PB -1 SoAm /NoAm

C

51.7

115

178

241

304

367

431

494

557

620

CDFM

21L.

1_Se

ub_H

olar

ctic

Y84

6_yH

QL5

60_F

RUIT

_Sce

rXSk

udXS

eub

CitK

P_yH

QL6

94_F

RUIT

_lag

erSa

azY

1264

6_yH

QL5

72_F

RUIT

_Suv

aXSe

ubY

1527

_yHQ

L580

_FRU

IT_S

uvaX

Seub

Y12

693_

FM47

1_BE

ER_l

ager

Saaz

WLP

862_

yHQ

L618

_BEE

R_la

ger

WY2

042_

yHQ

L627

_BEE

R_la

ger

yHRV

M10

7_Se

ub_H

olar

ctic

yHRV

M10

8_Se

ub_H

olar

ctic

yHKS

509_

Seub

_PB1

yHRV

M83

_Seu

b_PB

1P1

C1_S

eub_

PB1

yHAB

575_

NR7

_Seu

b_PB

1yH

AB57

6_N

R9_S

eub_

PB1

yHAB

121_

CRUB

2058

_Seu

b_PB

1yH

AB93

_CRU

B203

0_Se

ub_P

B1yH

CT53

_CRU

B193

8_Se

ub_P

B1yH

AB71

_CRU

B200

9_Se

ub_P

B1yH

CT94

_CRU

B196

4_Se

ub_P

B1yH

AB50

5_TC

64_S

eub_

PB1

yHAB

61_C

RUB2

001_

Seub

_PB1

yHAB

75_C

RUB1

582_

Seub

_PB1

yHCT

62_C

RUB1

593_

Seub

_PB1

yHCT

92_C

RUB1

962_

Seub

_PB1

yHAB

65_C

RUB1

575_

Seub

_PB1

yHCT

61_C

RUB1

576_

Seub

_PB1

yHAB

54_C

RUB1

995_

Seub

_PB1

yHCT

95_C

RUB1

965_

Seub

_PB1

yHAB

55_C

RUB1

996_

Seub

_PB1

yHAB

57_C

RUB1

998_

Seub

_PB1

yHAB

68_C

RUB1

579_

Seub

_PB1

yHCT

108_

CRUB

1581

_Seu

b_PB

1yH

CT93

_CRU

B196

3_Se

ub_P

B1yH

AB77

_CRU

B201

4_Se

ub_P

B1yH

AB59

_CRU

B200

0_Se

ub_P

B1yH

AB62

_CRU

B200

2_Se

ub_P

B1yH

CT12

0_CR

UB19

86_S

eub_

PB1

yHCT

87_C

RUB1

957_

Seub

_PB1

yHCT

98_C

RUB1

968_

Seub

_PB1

yHKB

35_S

eub_

PB1

yHCT

63_C

RUB1

761_

Seub

_PB1

yHAB

97_C

RUB2

034_

Seub

_PB1

yHCT

69_C

RUB1

940_

Seub

_PB1

yHAB

100_

CRUB

2037

_Seu

b_PB

1yH

AB99

_CRU

B203

6_Se

ub_P

B1yH

AB57

0_CB

72

yHAB

571_

CB8

5_Se

ub_P

B1yH

AB57

3_CB

95_

Seub

_PB1

yHAB

572_

CB9

2_Se

ub_P

B1yH

CT16

0_CR

UB15

68_S

eub_

PB1

yHCT

129_

1568

.2_S

eub_

PB1

yHCT

76_C

RUB1

568T

_Seu

b_PB

1yH

CT48

_CRU

B193

1_Se

ub_P

B1yH

AB10

7_CR

UB20

44_S

eub_

PB1

yHAB

89_C

RUB2

026_

Seub

_PB1

yHAB

109_

CRUB

2046

_Seu

b_PB

1yH

AB48

9_TC

48_S

eub_

PB1

yHAB

108_

CRUB

2045

_Seu

b_PB

1yH

AB87

_CRU

B202

4_Su

vaXS

eub

yHAB

88_C

RUB2

025_

Suva

XSeu

byH

AB96

_CRU

B203

3_Se

ub_P

B1yH

CT50

_CRU

B193

3_Se

ub_P

B1yH

CT64

_CRU

B176

2_Se

ub_P

B1yH

CT75

_CRU

B194

6_Se

ub_P

B1yH

CT51

_Suv

aXSe

ubyH

CT10

6_CR

UB19

76_S

uvaX

Seub

yHAB

90_C

RUB2

027_

Seub

_PB1

yHAB

91_C

RUB2

028_

Seub

_PB1

yHCT

49_C

RUB1

932_

Seub

_PB1

yHCT

84_C

RUB1

954_

Seub

_PB1

yHAB

105_

CRUB

2042

_Seu

b_PB

3yH

CT10

2_CR

UB19

72_S

eub_

PB3

yHAB

116_

CRUB

2053

_Seu

b_PB

1yH

CT57

_CRU

B195

0_Se

ub_P

B1yH

AB11

7_CR

UB20

54_S

eub_

PB1

yHAB

106_

CRUB

2043

_Seu

b_PB

1yH

CT11

6_CR

UB19

82_S

eub_

PB1

yHCT

47_C

RUB1

930_

Seub

_PB1

yHAB

566_

B33

5_Se

ub_P

B3yH

AB56

4_B3

13_

Seub

_PB3

yHCT

119_

CRUB

1985

_Seu

b_PB

2yH

QL7

26_N

PCC1

445_

Seub

_PB2

yHQ

L738

_NPC

C129

7_Se

ub_P

B2yH

QL7

32_N

PCC1

294_

Seub

_PB2

yHQ

L736

_NPC

C144

0_Se

ub_P

B2yH

CT10

7_CR

UB19

77_S

eub_

PB2

yHAB

110_

CRUB

2047

_Seu

b_PB

2yH

AB11

1_CR

UB20

48_S

eub_

PB2

yHCT

70_C

RUB1

941_

Seub

_PB2

yHCT

71_C

RUB1

942_

Seub

_PB2

yHQ

L744

_NPC

C131

1_Se

ub_P

B2yH

QL7

58_N

PCC1

292_

Seub

_PB2

yHQ

L743

_NPC

C144

4_Se

ub_P

B2yH

QL7

47_N

PCC1

301_

Seub

_PB2

yHQ

L733

_NPC

C144

2_Se

ub_P

B2yH

AB12

4_CR

UB20

61_S

eub_

PB2

yHAB

126_

CRUB

2062

_Seu

b_PB

2yH

AB56

_CRU

B199

7_Se

ub_P

B2yH

CT11

7_CR

UB19

83_S

eub_

PB2

yHCT

97_C

RUB1

967_

Seub

_PB2

yHCT

91_C

RUB1

961_

Seub

_PB2

yHCT

88_C

RUB1

958_

Seub

_PB2

yHAB

66_C

RUB2

005_

Seub

_PB2

yHAB

74_C

RUB2

012_

Seub

_PB2

yHAB

67_C

RUB2

006_

Seub

_PB2

yHCT

89_C

RUB1

959_

Seub

_PB2

yHCT

100_

CRUB

1970

_Seu

b_PB

2yH

AB12

5_CR

UB18

92_S

eub_

PB2

yHAB

565_

B32

1_Se

ub_P

B3yH

CT10

5_CR

UB19

75_S

eub_

PB3

yHCT

115_

CRUB

1981

_Seu

b_PB

3yH

AB69

_CRU

B200

7_Se

ub_P

B3yH

AB78

_CRU

B201

5_Se

ub_P

B3yH

AB80

_CRU

B201

7_Se

ub_P

B3yH

AB12

0_CR

UB20

57_S

eub_

PB3

yHAB

113_

CRUB

2050

_Seu

b_PB

3yH

AB11

5_CR

UB20

52_S

eub_

PB3

yHAB

86_C

RUB2

023_

Seub

_PB3

yHCT

113_

S14

1_Se

ub_P

B3yH

AB11

2_CR

UB20

49_S

eub_

PB3

yHAB

118_

CRUB

2055

_Seu

b_PB

3yH

CT66

_CRU

B193

5_Se

ub_P

B3yH

CT59

_CRU

B195

2_Se

ub_P

B3yH

CT58

_CRU

B195

1_Se

ub_P

B3yH

AB84

_CRU

B202

1_Se

ub_P

B3yH

AB85

_CRU

B202

2_Se

ub_P

B3yH

CT56

_CRU

B194

9_Se

ub_P

B3yH

AB49

1_TC

50_S

eub_

PB3

yHCT

52_C

RUB1

936_

Seub

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yHAB

114_

CRUB

2051

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b_PB

3yH

AB82

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B201

9_Se

ub_P

B3yH

AB81

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B201

8_Se

ub_P

B3yH

AB12

2_CR

UB20

59_S

eub_

PB3

yHAB

83_C

RUB2

020_

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60_C

RUB1

953_

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yHCT

112_

S13

1_Se

ub_P

B3yH

AB92

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B202

9_Se

ub_P

B3yH

CT54

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B194

7_Se

ub_P

B3yH

CT55

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B194

8_Se

ub_P

B3yH

QL7

30_N

PCC1

286_

Seub

_PA2

yHAB

94_C

RUB2

031_

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yHQ

L755

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C129

6_Se

ub_P

A2yH

AB70

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B200

8_Se

ub_P

A2yH

AB57

7_B3

91_

Seub

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yHAB

102_

CRUB

2039

_Seu

b_PA

2yH

AB10

1_CR

UB20

38_S

eub_

PA2

yHAB

103_

CRUB

2040

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b_PA

2yH

AB10

4_CR

UB20

41_S

eub_

PA2

yHCT

68_C

RUB1

939_

Seub

_PA2

yHAB

567_

B35

5_Se

ub_P

A2yH

AB56

8_B3

56_

Seub

_PA2

yHCT

46_C

RUB1

929_

Seub

_PA2

yHCT

99_C

RUB1

969_

Seub

_PA2

yHCT

90_C

RUB1

960_

Seub

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yHQ

L710

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C144

1_Se

ub_P

A2yH

QL7

09_N

PCC1

291_

Seub

_PA2

yHQ

L717

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C144

3_Se

ub_P

A2yH

AB63

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B200

3_Se

ub_P

A2yH

AB95

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B203

2_Se

ub_P

A2yH

AB79

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B201

6_Se

ub_P

A2yH

CT11

4_CR

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80_S

eub_

PA2

yHAB

119_

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2056

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b_PA

2yH

CT72

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B194

3_Se

ub_P

A2yH

QL7

08_N

PCC1

285_

Seub

_PA2

yHQ

L705

_NPC

C143

9_Se

ub_P

A2yH

QL7

15_N

PCC1

284_

Seub

_PA2

yHQ

L740

_NPC

C128

2_Se

ub_P

A2yH

QL7

27_N

PCC1

287_

Seub

_PA2

yHQ

L714

_NPC

C142

9_Se

ub_P

A2yH

QL7

51_N

PCC1

430_

Seub

_PA2

yHQ

L754

_NPC

C143

5_Se

ub_P

A2yH

QL7

29_N

PCC1

431_

Seub

_PA2

yHQ

L756

_NPC

C143

2_Se

ub_P

A2yH

QL7

75_N

PCC1

437_

Seub

_PA2

yHAB

73_C

RUB2

011_

Seub

_PA1

yHCT

96_C

RUB1

966_

Seub

_PA1

yHAB

58_C

RUB1

999_

Seub

_PA1

yHAB

569_

B36

6_Se

ub_P

A1yH

AB64

_CRU

B200

4_Se

ub_P

A1yH

CT10

1_Ex

CR10

7b_S

eub_

PA1

yHCT

103_

CRUB

1973

_Seu

b_PA

1yH

AB57

4_Q

C15_

Seub

_PA1

yHAB

76_C

RUB2

013_

Seub

_PA1

yHCT

104_

CRUB

1974

_Seu

b_PA

1yH

AB57

8_C3

94_

Seub

_SoA

myH

DPN

424_

LL20

1322

1_Se

ub_A

dmix

_NoA

myH

KS68

9_Se

ub_A

dmix

_NoA

myH

KS21

0_Se

ub_A

dmix

_NoA

myH

KS21

2_Se

ub_A

dmix

_NoA

myH

DPN

422_

LL20

1321

9_Se

ub_A

dmix

_NoA

myH

KB24

6_Se

ub_A

dmix

_NoA

myH

KS57

6_Se

ub_A

dmix

_NoA

myH

KS69

4_Se

ub_A

dmix

_NoA

myH

KB21

0_Se

ub_A

dmix

_NoA

myH

KB20

1_Se

ub_A

dmix

_NoA

myH

KS21

1_Se

ub_A

dmix

_NoA

myH

KB25

1_Se

ub_A

dmix

_NoA

myH

KB21

8_Se

ub_A

dmix

_NoA

myH

DPN

421_

LL20

1321

8_Se

ub_A

dmix

_NoA

myH

DPN

423_

LL20

1322

0_Se

ub_A

dmix

_NoA

myH

KB26

8_Se

ub_A

dmix

_NoA

myH

KB24

2_Se

ub_A

dmix

_NoA

myH

KS81

0_Se

ub_A

dmix

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myH

KS81

2_Se

ub_A

dmix

_NoA

myH

QL1

481_

Seub

_Adm

ix_N

oAm

yHQ

L162

1_Se

ub_A

dmix

_NoA

m

CDFM21L.1_Seub_HolarcticY 846_yHQL560_FRUIT_ScerXSkudXSeubCitKP_yHQL694_FRUIT_lager SaazY 12646_yHQL572_FRUIT_SuvaXSeubY 1527_yHQL580_FRUIT_SuvaXSeubY 12693_FM471_BEER_lager SaazWLP862_yHQL618_BEER_lagerWY2042_yHQL627_BEER_lageryHRVM107_Seub_HolarcticyHRVM108_Seub_HolarcticyHKS509_Seub_PB1yHRVM83_Seub_PB1P1C1_Seub_PB1yHAB575_NR7_Seub_PB1yHAB576_NR9_Seub_PB1yHAB121_CRUB2058_Seub_PB1yHAB93_CRUB2030_Seub_PB1yHCT53_CRUB1938_Seub_PB1yHAB71_CRUB2009_Seub_PB1yHCT94_CRUB1964_Seub_PB1yHAB505_TC64_Seub_PB1yHAB61_CRUB2001_Seub_PB1yHAB75_CRUB1582_Seub_PB1yHCT62_CRUB1593_Seub_PB1yHCT92_CRUB1962_Seub_PB1yHAB65_CRUB1575_Seub_PB1yHCT61_CRUB1576_Seub_PB1yHAB54_CRUB1995_Seub_PB1yHCT95_CRUB1965_Seub_PB1yHAB55_CRUB1996_Seub_PB1yHAB57_CRUB1998_Seub_PB1yHAB68_CRUB1579_Seub_PB1yHCT108_CRUB1581_Seub_PB1yHCT93_CRUB1963_Seub_PB1yHAB77_CRUB2014_Seub_PB1yHAB59_CRUB2000_Seub_PB1yHAB62_CRUB2002_Seub_PB1yHCT120_CRUB1986_Seub_PB1yHCT87_CRUB1957_Seub_PB1yHCT98_CRUB1968_Seub_PB1yHKB35_Seub_PB1yHCT63_CRUB1761_Seub_PB1yHAB97_CRUB2034_Seub_PB1yHCT69_CRUB1940_Seub_PB1yHAB100_CRUB2037_Seub_PB1yHAB99_CRUB2036_Seub_PB1yHAB570_CB7 2yHAB571_CB8 5_Seub_PB1yHAB573_CB9 5_Seub_PB1yHAB572_CB9 2_Seub_PB1yHCT160_CRUB1568_Seub_PB1yHCT129_1568.2_Seub_PB1yHCT76_CRUB1568T_Seub_PB1yHCT48_CRUB1931_Seub_PB1yHAB107_CRUB2044_Seub_PB1yHAB89_CRUB2026_Seub_PB1yHAB109_CRUB2046_Seub_PB1yHAB489_TC48_Seub_PB1yHAB108_CRUB2045_Seub_PB1yHAB87_CRUB2024_SuvaXSeubyHAB88_CRUB2025_SuvaXSeubyHAB96_CRUB2033_Seub_PB1yHCT50_CRUB1933_Seub_PB1yHCT64_CRUB1762_Seub_PB1yHCT75_CRUB1946_Seub_PB1yHCT51_SuvaXSeubyHCT106_CRUB1976_SuvaXSeubyHAB90_CRUB2027_Seub_PB1yHAB91_CRUB2028_Seub_PB1yHCT49_CRUB1932_Seub_PB1yHCT84_CRUB1954_Seub_PB1yHAB105_CRUB2042_Seub_PB3yHCT102_CRUB1972_Seub_PB3yHAB116_CRUB2053_Seub_PB1yHCT57_CRUB1950_Seub_PB1yHAB117_CRUB2054_Seub_PB1yHAB106_CRUB2043_Seub_PB1yHCT116_CRUB1982_Seub_PB1yHCT47_CRUB1930_Seub_PB1yHAB566_B33 5_Seub_PB3yHAB564_B31 3_Seub_PB3yHCT119_CRUB1985_Seub_PB2yHQL726_NPCC1445_Seub_PB2yHQL738_NPCC1297_Seub_PB2yHQL732_NPCC1294_Seub_PB2yHQL736_NPCC1440_Seub_PB2yHCT107_CRUB1977_Seub_PB2yHAB110_CRUB2047_Seub_PB2yHAB111_CRUB2048_Seub_PB2yHCT70_CRUB1941_Seub_PB2yHCT71_CRUB1942_Seub_PB2yHQL744_NPCC1311_Seub_PB2yHQL758_NPCC1292_Seub_PB2yHQL743_NPCC1444_Seub_PB2yHQL747_NPCC1301_Seub_PB2yHQL733_NPCC1442_Seub_PB2yHAB124_CRUB2061_Seub_PB2yHAB126_CRUB2062_Seub_PB2yHAB56_CRUB1997_Seub_PB2yHCT117_CRUB1983_Seub_PB2yHCT97_CRUB1967_Seub_PB2yHCT91_CRUB1961_Seub_PB2yHCT88_CRUB1958_Seub_PB2yHAB66_CRUB2005_Seub_PB2yHAB74_CRUB2012_Seub_PB2yHAB67_CRUB2006_Seub_PB2yHCT89_CRUB1959_Seub_PB2yHCT100_CRUB1970_Seub_PB2yHAB125_CRUB1892_Seub_PB2yHAB565_B32 1_Seub_PB3yHCT105_CRUB1975_Seub_PB3yHCT115_CRUB1981_Seub_PB3yHAB69_CRUB2007_Seub_PB3yHAB78_CRUB2015_Seub_PB3yHAB80_CRUB2017_Seub_PB3yHAB120_CRUB2057_Seub_PB3yHAB113_CRUB2050_Seub_PB3yHAB115_CRUB2052_Seub_PB3yHAB86_CRUB2023_Seub_PB3yHCT113_S14 1_Seub_PB3yHAB112_CRUB2049_Seub_PB3yHAB118_CRUB2055_Seub_PB3yHCT66_CRUB1935_Seub_PB3yHCT59_CRUB1952_Seub_PB3yHCT58_CRUB1951_Seub_PB3yHAB84_CRUB2021_Seub_PB3yHAB85_CRUB2022_Seub_PB3yHCT56_CRUB1949_Seub_PB3yHAB491_TC50_Seub_PB3yHCT52_CRUB1936_Seub_PB3yHAB114_CRUB2051_Seub_PB3yHAB82_CRUB2019_Seub_PB3yHAB81_CRUB2018_Seub_PB3yHAB122_CRUB2059_Seub_PB3yHAB83_CRUB2020_Seub_PB3yHCT60_CRUB1953_Seub_PB3yHCT112_S13 1_Seub_PB3yHAB92_CRUB2029_Seub_PB3yHCT54_CRUB1947_Seub_PB3yHCT55_CRUB1948_Seub_PB3yHQL730_NPCC1286_Seub_PA2yHAB94_CRUB2031_Seub_PA2yHQL755_NPCC1296_Seub_PA2yHAB70_CRUB2008_Seub_PA2yHAB577_B39 1_Seub_PA2yHAB102_CRUB2039_Seub_PA2yHAB101_CRUB2038_Seub_PA2yHAB103_CRUB2040_Seub_PA2yHAB104_CRUB2041_Seub_PA2yHCT68_CRUB1939_Seub_PA2yHAB567_B35 5_Seub_PA2yHAB568_B35 6_Seub_PA2yHCT46_CRUB1929_Seub_PA2yHCT99_CRUB1969_Seub_PA2yHCT90_CRUB1960_Seub_PA2yHQL710_NPCC1441_Seub_PA2yHQL709_NPCC1291_Seub_PA2yHQL717_NPCC1443_Seub_PA2yHAB63_CRUB2003_Seub_PA2yHAB95_CRUB2032_Seub_PA2yHAB79_CRUB2016_Seub_PA2yHCT114_CRUB1980_Seub_PA2yHAB119_CRUB2056_Seub_PA2yHCT72_CRUB1943_Seub_PA2yHQL708_NPCC1285_Seub_PA2yHQL705_NPCC1439_Seub_PA2yHQL715_NPCC1284_Seub_PA2yHQL740_NPCC1282_Seub_PA2yHQL727_NPCC1287_Seub_PA2yHQL714_NPCC1429_Seub_PA2yHQL751_NPCC1430_Seub_PA2yHQL754_NPCC1435_Seub_PA2yHQL729_NPCC1431_Seub_PA2yHQL756_NPCC1432_Seub_PA2yHQL775_NPCC1437_Seub_PA2yHAB73_CRUB2011_Seub_PA1yHCT96_CRUB1966_Seub_PA1yHAB58_CRUB1999_Seub_PA1yHAB569_B36 6_Seub_PA1yHAB64_CRUB2004_Seub_PA1yHCT101_ExCR10 7b_Seub_PA1yHCT103_CRUB1973_Seub_PA1yHAB574_QC15_Seub_PA1yHAB76_CRUB2013_Seub_PA1yHCT104_CRUB1974_Seub_PA1yHAB578_C39 4_Seub_SoAmyHDPN424_LL2013 221_Seub_Admix_NoAmyHKS689_Seub_Admix_NoAmyHKS210_Seub_Admix_NoAmyHKS212_Seub_Admix_NoAmyHDPN422_LL2013 219_Seub_Admix_NoAmyHKB246_Seub_Admix_NoAmyHKS576_Seub_Admix_NoAmyHKS694_Seub_Admix_NoAmyHKB210_Seub_Admix_NoAmyHKB201_Seub_Admix_NoAmyHKS211_Seub_Admix_NoAmyHKB251_Seub_Admix_NoAmyHKB218_Seub_Admix_NoAmyHDPN421_LL2013 218_Seub_Admix_NoAmyHDPN423_LL2013 220_Seub_Admix_NoAmyHKB268_Seub_Admix_NoAmyHKB242_Seub_Admix_NoAmyHKS810_Seub_Admix_NoAmyHKS812_Seub_Admix_NoAmyHQL1481_Seub_Admix_NoAmyHQL1621_Seub_Admix_NoAm

PAAd

mix

AdmixPB -1 PB -2 PB -3 PA -1PA -2

PB

Holarctic & Hybrids


https://doi.org/10.1101/709535


● ●

●● ● ● ● ●

●● ●

●●●●

●●

●

●●

FT HS

−15

−10

−5

0

5

subPop

Rec

over

y Po

st S

tress

subPop●●

●●

●●

●●

●●

●●

●●

●●

PA−1

PA−2

NoAm

PB−1

PB−2

PB−3

Holarctic

Lager

Figure S2A

●●

●

●

● ●●●

●

●

●

●

●●● ●

●●

●●

●

●

●●● ●●●

●

●

●●●●● ●●●

●●

0C 4C 10C 20C

1e−04

1e−03

1e−02

1e−01

subPop

log(

Gro

wth

Rat

e)

subPop●●

●●

●●

●●

●●

●●

●●

●●

PA−1

PA−2

NoAm

PB−1

PB−2

PB−3

Holarctic

Lager

● ●

●

●

● ●

● ●

●●

●

●

●● ●

●●

●

●●

●

●

●● ●

● ●

●

●●●

●●

●

●

●

●●

Galactose Glucose Maltose Raffinose

0.00

0.02

0.04

0.06

0.08

Subpop

Gro

wth

Rat

e

Subpop●●

●●

●●

●●

●●

●●

●●

●●

PA−1

PA−2

NoAm

PB−1

PB−2

PB−3

Holarctic

Lager

●

●

●●

●●

●

●

●●

●●

● ● ●●

●

●

● ●● ●

●●

●●

●

Ethanol Glycerol Maltotriose

0.000

0.005

0.010

0.015

0.020

Subpop

Gro

wth

Rat

e

Subpop●●

●●

●●

●●

●●

●●

●●

●●

PA−1

PA−2

NoAm

PB−1

PB−2

PB−3

Holarctic

Lager

*

*

*C

B

Holarctic:10C

Holarctic:20C

Holarctic:4C

Lager:0C

Lager:10C

Lager:20C

Lager:4C

NoAm:0C

NoAm:10C

NoAm:20C

NoAm:4C

PA−1:0C

PA−1:10C

PA−1:20C

PA−1:4C

PA−2:0C

PA−2:10C

PA−2:20C

PA−2:4C

PB−1:0C

PB−1:10C

PB−1:20C

PB−1:4C

PB−2:0C

PB−2:10C

PB−2:20C

PB−2:4C

PB−3:0C

PB−3:10C

PB−3:20C

PB−3:4C

Holarctic:0C

Holarctic:10C

Holarctic:20C

Holarctic:4C

Lager:0C

Lager:10C

Lager:20C

Lager:4C

NoAm:0C

NoAm:10C

NoAm:20C

NoAm:4C

PA−1:0C

PA−1:10C

PA−1:20C

PA−1:4C

PA−2:0C

PA−2:10C

PA−2:20C

PA−2:4C

PB−1:0C

PB−1:10C

PB−1:20C

PB−1:4C

PB−2:0C

PB−2:10C

PB−2:20C

PB−2:4C

PB−3:0C

PB−3:10C

PB−3:20C

Subpop|Temperature

Subpop|Tem

perature

−0.1

0.0

0.1

diff

Holarctic:GalactoseHolarctic:GlucoseHolarctic:GlycerolHolarctic:Maltose

Holarctic:MaltotrioseHolarctic:Raffinose

Lager:EthanolLager:GalactoseLager:GlucoseLager:GlycerolLager:Maltose

Lager:MaltotrioseLager:RaffinoseNoAm:Ethanol

NoAm:GalactoseNoAm:GlucoseNoAm:GlycerolNoAm:Maltose

NoAm:MaltotrioseNoAm:RaffinosePA−1:Ethanol

PA−1:GalactosePA−1:GlucosePA−1:GlycerolPA−1:Maltose

PA−1:MaltotriosePA−1:RaffinosePA−2:Ethanol

PA−2:GalactosePA−2:GlucosePA−2:GlycerolPA−2:Maltose

PA−2:MaltotriosePA−2:RaffinosePB−1:Ethanol

PB−1:GalactosePB−1:GlucosePB−1:GlycerolPB−1:Maltose

PB−1:MaltotriosePB−1:RaffinosePB−2:Ethanol


PB−2:MaltotriosePB−2:RaffinosePB−3:Ethanol


PB−3:MaltotriosePB−3:Raffinose

Holarctic:Ethanol

Holarctic:Galactose

Holarctic:Glucose

Holarctic:Glycerol

Holarctic:Maltose

Holarctic:Maltotriose

Holarctic:Raffinose

Lager:E

thanol

Lager:G

alactose

Lager:G

lucose

Lager:G

lycerol

Lager:M

altose

Lager:M

altotriose

Lager:R

affinose

NoAm:Ethanol

NoAm:Galactose

NoAm:Glucose

NoAm:Glycerol

NoAm:Maltose

NoAm:Maltotriose

NoAm:Raffinose

PA−1:Ethanol

PA−1:Galactose

PA−1:Glucose

PA−1:Glycerol

PA−1:Maltose

PA−1:Maltotriose

PA−1:Raffinose

PA−2:Ethanol

PA−2:Galactose

PA−2:Glucose

PA−2:Glycerol

PA−2:Maltose

PA−2:Maltotriose

PA−2:Raffinose

PB−1:Ethanol

PB−1:Galactose

PB−1:Glucose

PB−1:Glycerol

PB−1:Maltose

PB−1:Maltotriose

PB−1:Raffinose

PB−2:Ethanol

PB−2:Galactose

PB−2:Glucose

PB−2:Glycerol

PB−2:Maltose

PB−2:Maltotriose

PB−2:Raffinose

PB−3:Ethanol

PB−3:Galactose

PB−3:Glucose

PB−3:Glycerol

PB−3:Maltose

PB−3:Maltotriose

Subpop|Carbon

Subpop|Carbon

−0.03

0.00

0.03

diff

E

D

*

*

* **

***

***

**

●

●

●●

●●

●

●

●●

●●

● ● ●●

●

●

● ●● ●

●●

●●

●


0.000

0.005

0.010

0.015

0.020

Subpop

Gro

wth

Rat

e

Subpop●●

●●

●●

●●

●●

●●

●●

●●

PA−1

PA−2

NoAm

PB−1

PB−2

PB−3

Holarctic

Lager

●

●

●●

●●

●

●

●●

●●

● ● ●●

●

●

● ●● ●

●●

●●

●


0.000

0.005

0.010

0.015

0.020

Subpop

Gro

wth

Rat

e

Subpop●●

●●

●●

●●

●●

●●

●●

●●

PA−1

PA−2

NoAm

PB−1

PB−2

PB−3

Holarctic

Lager


https://doi.org/10.1101/709535


●●

● ●●● ●● ●●●●

●●●●● ●●● ●

●●● ●

●● ●● ●●● ● ● ●● ● ● ●

●

● ●●● ●●●●

●●●

● ●●

●●

●●●

● ● ●●

●●●

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●●●● ● ●● ●●●● ●● ●● ● ●●●● ● ●●

●

●

●● ●● ● ● ●●● ● ●●

●●

●●●

●

● ●● ●● ●●●

●●● ● ● ● ● ●● ●● ●

●

●●● ●● ●●●● ●● ●

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● ● ●● ●● ●●● ●● ● ●●● ●●●● ●● ●

● ●● ● ●●● ● ●● ●● ●●●●

0

50000

100000

Strain

Num

ber o

f SN

Ps

Subpop●

●

●

●

●

●

●

●

Holarctic

NoAm

PA−1

PA−2

PB−1

PB−2

PB−3

SoAm

PB−1

PB−2

PB−3

Holarctic

yHCT75yHCT75

−50

0

50

100

−50 0 50 100PC1 = 20.66%

PC2

= 14

.9%

popPB−1

PB−2

PB−3

Holarctic

SeubPopBintroPhase PCA

Figure S3

BA

C


https://doi.org/10.1101/709535


Figure S4

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●●●●● 0.64

PA−1PA−2

PB−2PB−3

Hol

NoAm

SoAm

I II III IV IXV VI VII VIII X XI XII XIII XIV XV XVI

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

Genome Position

F ST

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0.81

PA−1PA−2

PB−1PB−2

PB−3H

ol


0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

Genome Position

F ST

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https://doi.org/10.1101/709535


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●

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●●●●● 0.99

PA−1PA−2

PB−1PB−2

PB−3H

olN

oAm


0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

Genome Position

F ST

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● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ● ● ●●● ● ● ● ● ● ● ● ● ● ●●● ● ● ● ● ● ● ● ● ●● ● ● ● ● ● ● ● ● ●●●● ● ● ● ● ● ● ●●● ● ● ● ● ● ●●● ● ● ● ● ●●● ● ● ● ●● ● ● ● ●

●

●● ● ●●● ●●

●●●●● 0.99

PA−1PA−2

PB−1PB−2

PB−3H

olSoAm


0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

0.000.250.500.751.00

Genome Position

F ST


https://doi.org/10.1101/709535


Figure S6

PA−1PA−2

PB−1PB−2

PB−3H

ol


0

1

2

3

0

1

2

3

0

1

2

3

0

1

2

3

0

1

2

3

0

1

2

3

Genome Position

Avg

Pairw

ise

Dive

rgen

ce (%

)

0.0

0.5

1.0

1.5

I II III IV IXV VI VII VIII X XI XII XIII XIV XV XVIGenome Position

Avg

Pairw

ise

Dive

rgen

ce (%

)

−5

0

5

I II III IV IXV VI VII VIII X XI XII XIII XIV XV XVIGenome Position

log2

(Pai

rwis

e D

iverg

ence

BA

C


https://doi.org/10.1101/709535


yHCT51

yHCT106

yHAB88

yHAB87

0 200000 400000 600000

0 200000 400000 600000

0 200000 400000 600000

0 200000 400000 6000000

100

200

300

0

10

20

30

40

50

0

20

40

60

80

0

5

10

15

ChrXIV

Mea

n D

epth Species

Seub

Suva SA−A

SA−B

HOL

Australasia

yHAB87

yHAB88yHCT106

yHCT51

−10

0

10

20

30

−60 −40 −20 0PC1 = 52.77%

PC2

= 21

.81%

popAustralasia

HOL

Hybrid

SA−A

SA−B

SuvaSAintro PCA

PB−1

PB−2

PB−3

Holarctic

yHAB87

yHAB88yHCT51

yHCT106

−50

0

50

100

−50 0 50 100PC1 = 20.66%

PC2

= 14

.9%

popPB−1

PB−2

PB−3

Holarctic

SeubPopBintroPhase PCAFigure S7

0

5

10

15

Suva SeubGenome Position

Aver

age

Dep

th

SpeciesSeub

Suva

yHCT51

0

20

40

60


Aver

age

Dep

th

SpeciesSeub

Suva

yHCT106

0

100

200

300


Aver

age

Dep

th

SpeciesSeub

Suva

yHAB87

0

20

40


Aver

age

Dep

th

SpeciesSeub

Suva

yHAB88

B

AC

D


https://doi.org/10.1101/709535


0.001

0.002

0.003

0 500 1000 1500Distance (KM)

Nuc

leot

ide

Dive

rsity

(%)

0.0

0.1

0.2

0.3

0.4

0.5

0 5000 10000Distance (KM)

Nuc

leot

ide

Dive

rsity

(%)

Comparisons with Cerro Ñielol strains

Comparisons of SA strains with NZ, WA, and NC strains

Figure S8

BA


https://doi.org/10.1101/709535


Figure S9

Predicted Climatic Suitability without South American Sites

Longitude

Latitude

40°S

20°S

0°

20°N

40°N

60°N

150°W 100°W 50°W 0° 50°E 100°E 150°E

0.0

0.2

0.4

0.6

0.8

1.0

Predicted Climatic Suitability with Only South American Sites

Longitude

Latitude

40°S

20°S

0°

20°N

40°N

60°N

150°W 100°W 50°W 0° 50°E 100°E 150°E

0.0

0.2

0.4

0.6

0.8

1.0

B

Predicted Climatic Suitability Comparision of Three Different Strain Sets

Longitude

Latitude

40°S

20°S

0°

20°N

40°N

60°N

150°W 100°W 50°W 0° 50°E 100°E 150°E

0.0

0.5

1.0

1.5

2.0

2.5

3.0

C

A


https://doi.org/10.1101/709535


1 Genomic diversity and global distribution of Saccharomyces … · 88 (Peris et al. 2014, 2016;...

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