The coastal California Gnatcatcher controversy and how we determine distinctness of biological units

The coastal California Gnatcatcher controversy and how we determine

dis6nctness of biological units

John McCormack & James Maley Moore Lab of Zoology

Occidental College

We need sound science influencing land use policy

Ideally we’d base our decisions on science and

try to avoid litigation

But how do scien6sts determine the basic units of biodiversity?

•  We use natural history collections

•  We describe and analyze variation within and between populations

•  Using both genetics & appearance

FAQ: Why do you have to have so many of the same species?

Curators get this question a lot


The reason is that if you just had one from each of

two populations, they might look different …


But as you add specimens, you might find those

differences span the range of variation of each

population


Or you might find that the variation doesn’t overlap

at all*

*These represent extremes and it

is possible to detect significant

differences even when the values overlap some


Now imagine comparing many populations and

considering variation by sex and age --- you need a

lot of individuals to conduct a good study on

the units of biodiversity

The gnatcatcher controversy is a rare moment for

taxonomy in the limelight

Usually this only happens when a new species is

described, like the recent Perijá Tapaculo (Scytalopus

perijanus)

[Avendaño et al. 2015 Auk 132: 450]

Photo: USFWS

Talk Outline

•  coastal California Gnatcatchers

Talk Outline


•  Recommendations for describing subspecies

Talk Outline



•  Why philosophical debates in taxonomy matter to YOU

What is a “coastal” California Gnatcatcher?

It is the northern subspecies, designated as Threatened under the Endangered Species Act in 1993 based on distinct appearance &

taxonomic status as a subspecies

Polioptila californica californica

What is a “coastal” California Gnatcatcher?

It is the northern subspecies, designated as Threatened under the Endangered Species Act in 1993 based on distinct appearance &

taxonomic status as a subspecies

Polioptila californica californica Critical habitat

Patchy habitat in SoCal in coastal sage

scrub

There have been lots of eyes on this taxonomic issue


For example Alden Miller, Director MVZ


For example Alden Miller, Director MVZ

Dividing line generally set around

the 30 degree parallel

Your eyes on the problem

Photos courtesy of Phil Unitt at SDNHM

Thanks to natural history collections, you can see for yourself

Your eyes on the problem

Photos courtesy of Phil Unitt at SDNHM and Jen Gee

Thanks to natural history collections, you can see for yourself

californica has less white in the tail

And a darker back

From appearance to DNA


ATTGCTAGGTAGGG

ATTGCTAGGTAGGG

ATTACTAGGCAGGG

ATTACTAGGCAGGG

ATTACTAGGTAGGG

A stretch of DNA with individuals sharing some

mutations


ATTGCTAGGTAGGG

ATTGCTAGGTAGGG

ATTACTAGGCAGGG

ATTACTAGGCAGGG

ATTACTAGGTAGGG

You can generate a theory of

relatedness between groups and mark

where the changes occurred


ATTGCTAGGTAGGG

ATTGCTAGGTAGGG

ATTACTAGGCAGGG

ATTACTAGGCAGGG

ATTACTAGGTAGGG

Sometimes the genetic groups are coincident with geographic

areas


ATTGCTAGGTAGGG

ATTGCTAGGTAGGG

ATTACTAGGCAGGG

ATTACTAGGCAGGG

ATTACTAGGTAGGG

As with appearance, you can still detect differences among

populations even when populations contain mixes of genetic types


is to as is to

DNA has allowed new insight into evolutionary history, but this shouldn’t mean that we denigrate studies of appearance.

They are looking at two different kinds of variation --- one largely “neutral” and one potentially adaptive.


And often appearance and DNA corroborate the same story (though there are many exceptions)

Brown et al. 2007

Gene6cs of the gnatcatchers

•  Zink et al. 2000 looked at 1 mtDNA locus



•  1 DNA type (allele) was widespread




•  Rare alleles found in the south




•  Rare alleles found in the south

•  Petition to delist in 2010 rejected

•  USFWS asked for nuclear markers with high mutation rates

New study, new markers

•  Added 8 nuclear DNA regions •  Added one more mtDNA region



•  Added ecological climate modeling

–  Using temperature and rainfall data



•  Added ecological climate modeling

–  Using temperature and rainfall data

•  Conclusions

–  No genetic differences –  No ecological differences

Nuclear markers – the wrong ones Given what was already known from mtDNA, no

one would recommend looking at nuclear DNA loci at this taxonomic level --- not even Zink himself

There were no sta6s6cal tests for divergence

•  They eyeballed the geographic distributions of alleles looking for expected patterns

For one DNA region

Drawn from Zink’s 42-page comment to USFWS



Different DNA types & their relatedness Geographical location

of these types

For one DNA region




of these types

For one DNA region



•  Very qualitative



of these types

For one DNA region



•  Very qualitative •  Also the “expected

pattern” is wholly unrealistic –  More on this later



of these types

For one DNA region



•  Very qualitative •  Also the “expected

pattern” is wholly unrealistic –  More on this later

Actual expected pattern from Zink’s comment to USFWS

•  Last summer, a new petition to delist the gnatcatcher from the ESA was filed by the Pacific Legal Foundation

•  Reported in a story in the L.A. Times

•  190,000 acres potentially at stake (per L.A. Times)

In response to the story, and because I

had reviewed the study carefully, I

wrote a letter to the L.A. Times arguing that Zink et al. 2013

was not based on modern methods and

had little chance of finding differences

given their choice of markers and

ecological variables

This was headline writer’s word choice. I called the science second-rate, not

shoddy.

In response to the story, and because I

had reviewed the study carefully, I

wrote a letter to the L.A. Times arguing that Zink et al. 2013

was not based on the latest methods and had little chance of finding differences

given their choice of markers and

ecological variables

Zink and Barrowclough wrote

a reply letter

The editor of The Auk asked me to write a rebuttal paper


It was published in January with co-

author James Maley


It was published in January with co-

author James Maley

Free open access: http://www.bioone.org/doi/pdf/10.1642/AUK-14-184.1

Another look at the gene6c data in Zink et al. 2013

•  In addition to critiquing marker choice & their sweeping conclusions based on negative evidence



•  We conducted statistical tests (AMOVA) of the most simple hypothesis –  californica is different from south



•  We conducted statistical tests (AMOVA) of the most simple hypothesis –  californica is different from the rest

•  We did this because several loci showed private alleles in californica and frequency differences from south

Private alleles

Red allele more

common



•  We conducted statistical tests (AMOVA) of the most simple hypothesis –  californica is different from the rest

•  We did this because several loci showed private alleles in californica and frequency differences from south

•  AMOVA tests indicated 2 of 7 loci significantly differentiated between coastal CA gnatcatcher and south

Climate models use environmental data + species occurrence points to predict occupied habitats on a map

Digging into the ecological results



Environmental data comes from weather

stations and is interpolated over entire

globe





globe

Climate models overlap little between

coastals (gray) and south (black)

from Zink et al. 2013





globe

Climate models overlap little between

coastals (gray) and south (black)

So, different climates

--- but is this interesting?

from Zink et al. 2013

Let’s imagine a landscape spanning some geographic distance

N

Let’s call this north --- and we all know it’s generally hotter to the south

N

In the north the same trees you find at lower elevation…

N

… are found at higher elevation to the south

N

Now we can look at birds distributed over this gradient

N

We can take GPS points of birds from one area

Temperature

Ra

infa

ll N

Extract the climate data

and plot them

Temperature

Ra

infa

ll N

And do the same for the

birds from the other

area

Temperature

Ra

infa

ll N

Gee, look, they are

different. The thing is…

Temperature

Ra

infa

ll N

If you took GPS points from some rocks in the

areas…

Temperature

Ra

infa

ll N

And plotted them, they’d

look different too!

Temperature

Ra

infa

ll N

So how do we know these

differences

are important to the birds?

Temperature

Ra

infa

ll N

What we can do is take

many random

points from each area

Temperature

Ra

infa

ll N

And plot those

Temperature

Ra

infa

ll N

And ask: given what is

available, are the birds in

different habitats?

Temperature

Ra

infa

ll N

Despite desert being available, maybe birds to the south aren’t

found in the desert

Temperature

Ra

infa

ll N


found in the desert

Instead they are found in forest, like

the birds in the north

Temperature

Ra

infa

ll N


found in the desert

Instead they are found in forest, like

the birds in the north

This is called a conserved niche

Temperature

Ra

infa

ll N

Or maybe similar habitats

are available, but the birds

are in different habitats

Temperature

Ra

infa

ll N




Birds in south in desert despite

similar forest being available

Temperature

Ra

infa

ll N




This is called a divergent niche

Birds in south in desert despite

similar forest being available

Temperature

Ra

infa

ll N

Finally, you could fail to

reject the null hypothesis

Temperature

Ra

infa

ll N



And find that the birds are in habitats

that are about as different as the general regions where they live

Temperature

Ra

infa

ll N



And find that the birds are in habitats

that are about as different as the

regions where they live

In this case, you can’t disentangle whether the differences in their climate are truly important to the birds or whether it’s

just a trivial effect of living in different places

Temperature

Ra

infa

ll N

This latter case is what

Zink et al. 2013 found

Temperature

Ra

infa

ll N



They failed to reject the null

hypothesis

Temperature

Ra

infa

ll N



They failed to reject the null

hypothesis

Yet drew the sweeping conclusion that this meant the gnatcatchers are habitat generalists, which is

unsupported by their results

The differences in habitat between gnatcatchers is obvious

Coastal sage scrub

Cactus fields

Vegetation data can be obtained from remote sensing satellites

You don’t have to work at JPL to get these vegetation layers. You just have to care about looking everywhere you can for

differences.

Vegetation data can be obtained from remote sensing satellites

Talk Outline


How should we collect gene6c data? We are in a time of incredible new DNA sequencing

technology

We don’t have to rely on 8 DNA regions.

We can collect thousands.

We finally have gene6c techniques to probe the subspecies level

•  Wilson’s Warblers •  With mtDNA & other

nuclear loci only east and west distinct

Ruegg et al. 2014




•  Using 96 SNPs

•  Two subspecies in the western US also distinct

Ruegg et al. 2014




•  96 SNPs

•  Two subspecies in the western US also distinct

•  Other new methods that gather 1000s of DNA regions

•  Actually can gather neutral DNA and DNA controlling differences in appearance

Ruegg et al. 2014

How should we collect ecological data? In this case, there aren’t too many sites, so how about some

good old-fashioned, ecological field work? Or at least include vegetation layers.

How should we analyze differences in appearance? •  We know they look different

How should we analyze differences in appearance? •  We know they look different •  They only question is whether those

differences are “discrete”



Geographic distance

One smooth transition without discrete units



Geographic distance

One biological unit with a transition to another



Geographic distance

One biological unit with a transition to another

•  We now have great analytical methods for looking at geographic clines and testing their significance

Finally, the issue of funding source We said: Research should be carried out either free

from conflicts of interest or where such conflicts are

stated openly



stated openly

We know sponsorship bias exists

Source: Wikipedia



stated openly

We know sponsorship bias exists

It is likely subconscious or a form of publication bias Stating conflicts provides context to public, media, and

other scientists --- it does not mean a study is invalid

Source: Wikipedia

Zink et al. 2013 funding source

R. Thornton is a co-filer on the delisting petition

L.A. Times article said funding was from developers


Zink now denies study was funded by developers


Zink now denies study was funded by developers

Who “incorrectly implied” it?

It’s a direct quote in

quote marks from the

L.A. Times article. No

correction has been sought.

In any event, the fact that Robert Thornton is a lawyer who has defended developers’ interests has been known to Zink at least since 2005 when Thornton organized a conference and invited Zink to speak

So, if not developers, who did Robert Thornton secure the money from?

Again, conflicts don’t invalidate a study, but stating them openly is the right thing to do. The discrepancies

in the story and lack of transparency don’t instill trust.

Talk Outline

•  Why philosophical debates in taxonomy matter to YOU

Or why arcane philosophical debates over taxonomy matter to

YOU

In 2000, John Avise wrote a classic piece on a certain mental malady afflicting

some adherents of the Phylogenetic

Species Concept, called Cladists (big-C)

Background: We are all liWle-‐c cladists

Willi Hennig

Hennig invented cladistics & now we build the tree of life based on common

ancestors, not general similarity


Clade or monophyletic

group

Willi Hennig

Hennig invented cladistics & now we build the tree of life based on common

ancestors, not general similarity


Hard for the youngsters to believe phylogenies were ever done without cladistics, but apparently blood was spilled in the hallowed halls of our

natural history museums over all this

Images by David Maddison

Then big-‐C Cladists went off the rails

•  “Cladists” now known for extreme views –  If it’s not a clade, it

doesn’t exist

–  Parsimony rules

–  Models suck

Image by Sam Magruder

Then big-‐C Cladists went off the rails

•  “Cladists” now known for extreme views –  If it’s not a clade, it

doesn’t exist –  Parsimony rules –  Models suck

•  Obsession with clades fine for defining older taxonomic groups

•  Problems arise at and below the level of the species

Image by Sam Magruder

We don’t expect clades for subspecies

Time

Here’s the process of speciation!


Time

Populations split and begin to differ!


Time


They continue to exchange genes!


Time

Some go extinct; others fuse!




Time




Eventually gene exchange slows!


Time





Then stops!


Time





Then stops!

Far into future, all gene copies differ!


Time





Then stops!


Here’s the taxonomy!


Time





Then stops!


Most call these

subspecies or populations!


Time





Then stops!


Most call these


Debate over when to call species!


Time





Then stops!


Most call these


Debate over when to call species!

Cladist species!


Time

Cladist species!

Returning to Zink’s expected pattern, it’s

the most conservative anyone would apply for

SPECIES --- and would never be expected for subspecies!


What does a Cladist expect to find below the species level?!

Cladist expecta6ons?

What does a Cladist expect to find below the species level?!


Not sure, but they explicitly don’t consider processes like gene flow, so

this area describing

what’s happening is left blank!


Maybe they expect this, all neat

and clean?!

But then wouldn’t they just call these species?!


Maybe they expect this, all neat

and clean?!

If subspecies are defined by gene flow, can a big-C Cladist even believe in

subspecies?!


Take a moment to ponder this as the expected pattern of nuclear DNA loci for subspecies.!

!And what it would mean for defining

units of biodiversity under

the ESA.!

So you can collect genetic data until the cows come home.

“Ultimately this will complete the transition [to cladistic thinking] at ‘lower’ taxonomic scales [e.g., subspecies]. Until then the revolution in systematics and classification started by Hennig remains incomplete.” --- Bob Zink 1999

You won’t see the patterns if this is your viewpoint.

So you can collect genetic data until the cows come home.

If we let Cladists define the taxonomy of the Endangered Species Act…

If we let Cladists define the taxonomy of the Endangered Species Act…

…Then we really will be Through the Looking Glass.

Thanks

•  Oxy undergrad Emily Ridley

•  Kevin Winker and others provided invaluable advice

•  Our work was funded by an endowment to Occidental College by the late Robert T. and Margaret C. Moore

Photo courtesy of U.S. Fish & Wildlife Service.

Further reading •  John E. McCormack & James M. Maley 2015 Interpreting negative evidence

with taxonomic and conservation implications: another look at the distinctness of coastal California Gnatcatchers The Auk 132: 380-388 OPEN ACCESS: http://www.bioone.org/doi/pdf/10.1642/AUK-14-184.1

•  Michael A. Patten 2015 Subspecies and the philsophy of science The Auk 132: 481-485 OPEN ACCESS: http://www.bioone.org/doi/pdf/10.1642/AUK-15-1.1

•  Robert M. Zink et al. 2000 Genetics, taxonomy, and conservation of the threatened California gnatcatcher Conservation Biology 14: 1394-1405 http://onlinelibrary.wiley.com/doi/10.1046/j.1523-1739.2000.99082.x/full

•  Robert M. Zink et al. 2013 Phylogeography of the California Gnatcatcher (Polioptila californica) using multilocus DNA sequences and ecological niche modeling: implications for conservation The Auk 130: 449-458 OPEN ACCESS http://www.aoucospubs.org/doi/abs/10.1525/auk.2013.12241

•  Ornithological Monographs, No. 67 2010 [The Subspecies Issue] ALL ARTICLES OPEN ACCESS http://aoucospubs.org/doi/book/10.1525/aoum.67

The coastal California Gnatcatcher controversy and how we determine distinctness of biological units

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Transcript of The coastal California Gnatcatcher controversy and how we determine distinctness of biological units