Hybrid speciation with external barriers:(Asteraceae: Heliantheae), a case studyEncelia

Curtis Clark and Gerard J. AllanBiological Sciences, California State Polytechnic University, Pomona, and Rancho Santa Ana Botanic Garden

AbstractAbstractMost well-documented cases of homoploid hybrid speciation follow therecombinational model, in which the new species passes through a period ofgenetic rearrangement and reduced fertility. An alternate model has beenpresented, in which external barriers to gene flow prevent genetic swamping of thenew species by the parent species. The two documented cases of hybridspeciation in Encelia (E. virginensis and E. asperifolia) appear to follow this model.In both cases, the species of hybrid origin are morphologically intermediate to theparents, and E. virginensis is also similar to artificial F11 hybrids. In both cases, thespecies of hybrid origin share random amplified polymorphic DNA (RAPD) markerswith each of the parent species. A single sampled individual of each species ofhybrid origin combines the nrDNA internal transcribed spacer (ITS) sequences ofits parents. All North American Encelia species are obligate outcrossers with n =18 chromosomes, and in cultivation they form fertile hybrids apparently in allcombinations. In the natural environment, plants of F11 phenotype are locallycommon, but backcross progeny are rare, being confined primarily to areas ofhuman disturbance, and there is no evidence of introgression. Progeny tests in onecase of natural hybridisation suggested that backcross progeny are eliminated afterseed dispersal. This suggests that the F11 phenotype represents a “local optimum”on the selective landscape, and that the selection against backcrosses stronglyreduces gene flow between the incipient hybrid species and the parents.

Espèciation hybride avec barrières externes: Encelia (Asteraceae: Heliantheae), une étude de cas

La plupart des cas bien documentés de l’espèciation homoploïde hybride suivent le modèlerecombinaisonal, où l’espèce nouvelle passe par une durée de réarrangement génétique et lafertilité reduite. Un modèle alternatif a été présenté, où les barrières externes à flux génétiquedétournent la submersion génétique de l’espèce nouvelle par l’espèce parentale.Apparemment les deux cas documentés de l’espèciation hybride en Encelia (E. virginensis et E.asperifolia) suivent ce modèle. En tous les deux cas, les espèces d’origine hybride sontintermédiaire morphologiquement aux parents, et E. virginensis resemble aux hybridesartificielles F11. En tous les deux cases, les espèces d’origine hybride partagent indicateursrandom amplified polymorphic DNA (RAPD) avec chacun des espèces parentales. Un seulindividu échantillonné de chaque espèce d’origine hybride combine les séquences del’espacement interne transcrit de nrDNA (ITS) des parents. Toutes les espèces de Encelia enAmérique du Nord exigent la pollinisation extérieure et tiennent n = 18 chromosomes.Apparemment les hybrides fertiles forment en culture en toutes combinaisions. En milieunaturel, les plantes de phénotype F11 sont commun de lieu, mais les descendants revers-métis

(backcross) sont rare, étant limités surtout aux zones de perturbation anthropogénique, et iln’y a pas d’évidence d’introgression. En un cas d’hybridation naturelle, les épreuves de ladescendance suggérèrent que les descendants revers-métis sont éliminés après la dispersiondes séminaux. Ce suggére que le phénotype F11 représente un «optimum local» dans lepaysage sélectif, et que la sélection contre les descendants revers-métis réduit fortement leflux génétique entre l’espèce hybride nouvelle et ses parents.

The purpose of this poster is to propose that two species ofEncelia of hybrid origin conform to Grant’s “external barriers”model of hybrid speciation, rather than the better-known“recombinational” model. The species are E. virginensis A.Nels., derived from E. actoni Elmer and E. frutescens (A. Gray)A. Gray, and E. asperifolia (S.F. Blake) Clark & Kyhos, derivedfrom E. californica Nutt. and a glandular form of E. frutescens.

Both species satisfy the three criteria for recognition ofspecies of hybrid origin: intermediacy between the parents,similarity to F1 hybrids, and shared apomorphies with bothparents. Not all documented species of hybrid origin satisfy allthree criteria, and there is no theoretical reason that theyshould, but the nature of the speciation process outlined heremakes it more probable.

Encelia virginensis

E. actoni E. virginensis E. frutescensAlthough intermediate in many respects, is more easilyconfused with than .

E. virginensisE. actoni E. frutescens

E. actoni

E. virginensis

E. frutescens

California

Nevada Utah

Arizona

Sonora

Encelia actoni

Enceliafrutescens

Enceliavirginensis

inhabitsdesert mountains andthe western margins ofthe deserts.

is found inthe lowest Sonoran andMojave deserts.

occurs in thenortheastern MojaveDesert. It is sympatricwith its putative parentsin parts of its range.

Achene Length (mm)

6.0 6.5 7.0 7.5 8.0

Ach

ene

Wid

th (

mm

)

2.0

2.5

3.0

3.5

4.0

E. frutescens

E. virginensis

E. actoni

Mean Annual Range of Temperature (C)

10 15 20 25 30

Mea

n A

nn

ual

Tem

per

atu

re (

C)

10

15

20

25

30

Encelia actoni

Encelia virginensis

Encelia frutescens

The achenes of E. virgin-ensis are intermediate in length and width to those of the putative parents.

Encelia virginensis inhabitsregions with an inter-mediate mean temper-ature and a slightly more extreme range of temper-ature.

First Coordinate Axis

-20 -10 0 10 20 30 40

Sec

on

d C

oo

rdin

ate

Axi

s

-20

-10

0

10

20

E. virginensis

E. actoni

E. frutescens

length of petiolewidth of leafheight of headwidth of head

pedicel widthnumber of rayslength of raylength of leaf

Characters Used

A principal co-ordinate analysis based on eightcharacters of the leaves and heads shows E.virginensis to be generallyintermediate to its putativeparents.

0 200 400 600

E. actoni

E. virginensis

E. frutescens

Length (bases)

E. virginensis haschimeric ITS In the ITS region of the

nrDNA, anddiffer by 13

bases. The singleexaminedhas no unique bases,and shares the base ofone parent or the otherat all sites. The chartdepicts a scenario forthe chimeric DNA,assuming the minimumcrossing-over.

E. actoni E.frutescens

E. virginensis

Shared Apomorphies

E. actoni E. virginensis E. frutescensmorphological

broad, multicellular-based hairs

broad, multicellular-based hairs

RAPD

UBC 301 900bp UBC 301 900bp

UBC 301 600bp UBC 301 600bp

UBC 302 1200bp UBC 302 1200bp

(E. actoni has no clear morphological autapomorphies)

Encelia asperifolia

E. californica E. asperifolia E. frutescensglandular form

Encelia asperifolia E. californicais similar in appearance to ; it wasoriginally named as a variety of that species.

California Arizona

BajaCalifornia

E.californica

E. asperifolia

Encelia californica

E.frutescens

Enceliaasperifolia

E.californica

E. frutescens

lives incoastal sage scrub. Theglandular form of

inhabits thedry desert in the rainshadow of the northernmountains of BajaCalifornia.

is found in therocky coastal deserts ofBaja California. It isnarrowly sympatric to

, but allopatricto .

0 200 400 600

E. californica

E. asperifolia

Length (bases)

E. frutescens

In the ITS region of thenrDNA, and

differ by 21bases. The single exam-ined differsfrom either parent atthree of those sites, butshares the base of oneparent or the other at therest. The chart depicts ascenario for the chimericDNA, assuming mini-mum crossing-over. Thethree unique sites in

are in the redregion.

E. californicaE. frutescens

E. asperifolia

E.asperifolia

E. asperifolia haschimeric ITS

Shared Apomorphies

E. californica E. asperifolia E. frutescensmorphological

UV-reflective raycorollas

UV-reflective raycorollas

brown disk corollas brown disk corollas

moniliform hairs moniliform hairs

broad multicellular-based hairs

broad multicellular-based hairs

no benzopyrans orbenzofurans

no benzopyrans orbenzofurans

yellow stigmas yellow stigmas

Shared Apomorphies

E. californica E. asperifolia E. frutescensRAPD

UBC 218 800bp UBC 218 800bp

UBC 218 1600bp UBC 218 1600bp

UBC 382 1400bp UBC 382 1400bp

UBC 409 500bp UBC 409 500bp

UBC 478 1400bp UBC 478 1400bp

Operon B8 750bp Operon B8 750bp

UBC 149 700bp UBC 149 700bp

UBC 375 1000bp UBC 375 1000bp

The Encelia species described here clearly do not fit themodel of recombinational speciation:

Recombinational Model EnceliaChromosome differencesbetween parent species

No apparent chromosomedifferences between parents

Hybrids of reduced fertility,often uncomon

Hybrids of full fertility, oftencommon

Internal reproductive barriersbetween hybrids species andparent species

Fertile backcrosses arepossible, but eliminated inthe wild after seed dispersal

However, they do agree with Grant’s model of speciation

with external barriers.

Although Grant provided more examples of hybridspeciation with external barriers than of recombinationalspeciation, until recently most of the cases confirmed bymolecular evidence have been of the latter. Wolfe and Elisensre-examined Grant’s example from Penstemon, demonstratingthat, although the F11 hybrids had reduced fertility, externalbarriers, including floral differences that affect pollination,were important in maintaining the new species. In Encelia,hybrids have full fertility, so in a sense this represents anextreme case of this form of speciation. In addition, there areno floral isolating mechanisms in the genus. Kyhos et al.showed that backcross progeny in Encelia are routinelyproduced but almost never survive. This phenomenonprovides the necessary external barrier, although its basis isstill unknown.