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Extinction and Introgression in a Community of Partially Cross-Fertile Plant Species

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Extinction and Introgression in a Community of Partially Cross-Fertile Plant Species vol. 160, no. 1 the american naturalist july 2002 Extinction and Introgression in a Community of Partially Cross-Fertile Plant Species Jean-Baptiste Ferdy1,2,3,* and Fre´de´ric Austerlitz3,4,† 1. Department of Botany and Agricultural Biochemistry, frequency dependence and make extinction possible, even when hy- University of Vermont, Burlington, Vermont 05405; brid individuals have no intrinsic fitness advantage. 2. Conservatoire Botanique National du Bassin Parisien, Muse´um National d’Histoire Naturelle, 61, rue Buffon, F-75 005 Paris, Keywords: hybridization, genetic diversity, model, identity by descent, France; demography. 3. Laboratoire Evolution et Syste´matique, UPRESA 8079 Centre National de la Recherche Scientifique, Universite´ Paris-Sud, Baˆtiment 362, F-91 405 Orsay cedex, France; Hybridization between species or subspecies is a very com- 4. Department of Ecology, Evolution, and Natural Resources, mon phenomenon in plants and, to a smaller extent, in Cook College, Rutgers University, New Brunswick, New Jersey animals (Rhymer and Simberloff 1996). It can happen 08901-8551 naturally or as a consequence of accidental introduction Submitted August 20, 2001; Accepted December 7, 2001 or anthropogenically caused breakdown of natural barri- ers. This can lead, depending on the degree of reproductive isolation between the species, to either the extinction or the complete introgressive subversion of one species. Ex- amples of extinction by hybridization are reported by abstract: We develop a model to study the demography and ge- Levin et al. (1995) in island flora, in which endemic plant netics of an encounter between two partially cross-fertile plant spe- species hybridize with an introduced congener from a cies. We assume prezygotic reproductive isolation between the spe- cies, a common situation when the species differ by their phenology nearby continent. In some cases, hybridization does not or floral traits that cause assortative mating. Three outcomes are yield complete extinction of the endemic species, but after possible: coexistence of both species with minimal introgression; a few generations, the derivative population has a large domination by one species, with the other becoming extinct or sur- fraction of its gene pool derived from the introduced con- viving only through recurrent migration; or domination of the com- gener (Rhymer and Simberloff 1996). munity by hybrid derivatives, with both species surviving but with In such situations, genetic markers provide a tool to a rather high level of introgression between them. The first situation assess the level of introgression experienced by either spe- is reached when interfertility is low, while the third requires high cies. In some cases, the two species meet in a well-defined interfertility to develop. Occurrence of the second situation is ob- contact zone, and genetic markers define a cline across that served with intermediate values of interfertility. Gene flow from contact zone (Harrison and Bogdanowicz 1997; Goodman nearby monospecific populations can prevent both introgression and et al. 1999; Latta and Mitton 1999). The shape and steepness the domination of the community by one species. Conversely, in- creasing the number of loci that determine the reproductive isolation of the cline depend on the speed of diffusion of alleles between species or decreasing the degree of nonadditive interactions from one species into the other (Nichols and Hewitt 1994), (epistasis and/or dominance) between alleles and loci makes intro- and diffusion equations have been developed that yield a gression more likely. We found that hybridization can create positive good approximation of this speed (Barton and Gale 1993). The development of a cline, however, requires that gene * Corresponding author. Present address: Laboratoire Ge´nome, Populations, diversity follows an isolation-by-distance pattern (Nichols Interactions, Centre National de la Recherche Scientifique, Unite´ Mixte de and Hewitt 1994). In contrast, for species that can disperse Recherche 5000, Universite´ de Montpellier II, Montpellier, France; e-mail: for long distances or species with only few populations, a [email protected]. clinal pattern is not expected. Hybridization will lead to † Present address: Laboratoire de Ge´ne´tique et d’Ame´lioration des Arbres Forestiers, INRA, B.P. 45, Pierroton, F-33611 Gazinet cedex, France; e-mail: a few admixed populations rather than a recognizable [email protected]. cline. In this case, the distribution of genotypes can be Am. Nat. 2002. Vol. 160, pp. 74–86. ᭧ 2002 by The University of Chicago. bimodal, with the population comprising few hybrids and 0003-0147/2002/16001-0006$15.00. All rights reserved. being composed of individuals resembling one or the other Hybridization, Introgression, and Extinction 75 of the parent species, or unimodal, with the population boring populations of pure species. Thus, we can determine being then described as a hybrid swarm (Jiggins and Mallet the conditions under which one of the pure species or a 2000). hybrid form will invade the community, the conditions The aim of this work is to provide a model for the under which both species will coexist, and the level of processes leading to extinction of or introgression in hy- genetic introgression from one species into the other. bridizing populations and to describe the links between these processes and classical population genetic outcomes. To our knowledge, there has been only one attempt to Material and Methods model such a situation (Huxel 1999). Based on previous General Description of the Model work on Wright’s shifting balance theory (Crow et al. 1990; Kondrashov 1992), Huxel’s effort is a model in which the We assume that we have a community of constant size N difference between two species is determined by a single composed of hermaphroditic, self-fertile, diploid individ- biallelic locus, and it focuses on the probability of invasion uals belonging to two pure plant species, 0 and 1, and to of an initially rare (introduced) species. Models developed various hybrid forms. We assume that reproductive isolation for studying sympatric speciation (Kondrashov and Shpak between these two species is determined by nL independent 1998; Kondrashov and Kondrashov 1999) also yield some biallelic loci, with the two alleles denoted as ϩ and Ϫ. Based predictions about the outcome of a community consisting on the proportion of ϩ alleles an individual possesses, we p ϩ of several partially cross-fertile phenotypes. However, these definen 2n L01/(21 phenotypes P,PnL)1 , …,P , with the models concern only isolated populations. Moreover, in convention that the phenotypePk/(2nL) corresponds to the car- ϩ all these models, the fate of molecular markers that could rier of k alleles. Thus, phenotypes P0 and P1 are those of ≤ ≤ Ϫ introgress from one species to the other is not assessed. species 0 and 1, and phenotypes Pi for 1/(2n L) i 1 Here we develop a general deterministic model for the 1/(2n L) are hybrids in which the proportion of ancestry study of the transient dynamics and equilibrium states of from species 0 decreases when i increases (and, conversely, the demography and genetics within an admixed com- the proportion of ancestry from species 1 increases with munity that emerges from the encounter of two partially i). For the sake of simplicity, we will denote an individual interfertile plant species still linked through migration with of phenotype Pi as being of type i. Reproduction is pan- populations from their own species. We can thus inves- mictic among individuals of identical phenotype but is tigate the conditions leading to the extinction of one of partly prevented by prezygotic reproductive isolation be- the two species and how genetic differentiation between tween individuals of different phenotypes. The n pheno- the two species evolves under hybridization pressure; this types present in the community therefore define n ad- allows us to predict when meaningful introgression will mixture classes. The relative probability of an individual occur. of type j fertilizing an individual of type i is denoted hij We study the case in which reproductive isolation is and is computed as prezygotic. There are several biological situations in which p Ϫ F Ϫ F1Ϫe Ϫ ෈ this occurs. This is the case, for instance, for two interfertile hij 1 i j (1 h) i, j {0, … , 1}, (1) species with different phenologies. Mating chances would be reduced between early- and late-flowering individuals, where h is the interfertility between species 0 and 1 and and hybrids with intermediate phenology would primarily e is the degree of nonadditive interaction between the al- mate among themselves (Husband and Schemske 2000). leles and loci that determine the reproductive isolation Traits such as flower color (Smithson and Macnair 1997; between species 0 and 1. The casee p 0 therefore cor- Jones and Reithel 2001) or plant height (Peakall and Han- responds to the fully additive case. When e increases, re- del 1993) that cause assortative mating in flowering species productive isolation between two classes increases faster p with nonspecialized pollinators should create the same sort with the number of classes that separate them. If n L of situation. 1, e is the degree of dominance between the alleles of the We study the impact of several parameters on the tran- unique loci that determines reproductive isolation between sient dynamics and final equilibrium reached by the com- the two species. In the general case, e encapsulates both munity, starting with a situation in which the community dominance between the alleles of a loci and epistasis be- is composed only of the two pure species, that is, when tween loci. The calculation of hij when e and nL vary is the species meet for the first time. The parameters that we illustrated in figure 1. model are the level of interfertility between the two species, Once we know the probability that any types i and j the number of loci controlling this interfertility, the degree cross, we must determine the probability distribution of of nonadditive interaction between alleles (dominance) and the type of the offspring produced by that cross.
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