The Limits to Parapatric Speciation: Dobzhansky-Muller Incompatibilities in a Continent-Island Model (original) (raw)
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Gene flow tends to impede the accumulation of genetic divergence. Here, we determine the limits for the evolution of postzygotic reproductive isolation in a model of two populations that are connected by gene flow. We consider two selective mechanisms for the creation and maintenance of a genetic barrier: local adaptation leads to divergence among incipient species due to selection against migrants, and Dobzhansky-Muller incompatibilities (DMIs) reinforce the genetic barrier through selection against hybrids. In particular, we are interested in the maximum strength of the barrier under a limited amount of local adaptation, a challenge that may initially face many incipient species. We first confirm that with classical two-locus DMIs, the maximum amount of local adaptation is indeed a limit to the strength of a genetic barrier. However, with three or more loci and cryptic epistasis, this limit holds no longer. In particular, we identify a minimal configuration of three epistatically ...
Parapatric speciation in three islands: dynamics of geographical configuration of allele sharing
Royal Society open science, 2017
We studied the time to speciation by geographical isolation for a species living on three islands connected by rare migration. We assumed that incompatibility was controlled by a number of quantitative loci and that individuals differing in loci by more than a threshold did not mix genetically with each other. For each locus, we defined the geographical configuration (GC), which specifies islands with common alleles, and traced the stochastic transitions between different GCs. From these results, we calculated the changes in genetic distances. As a single migration event provides an opportunity for transitions in multiple loci, the GCs of different loci are correlated, which can be evaluated by constructing the stochastic differential equations of the number of loci with different GCs. Our model showed that the low number of incompatibility loci facilitates parapatric speciation and that migrants arriving as a group shorten the waiting time to speciation compared with the same numbe...
2017
We investigate the conditions for the origin and maintenance of postzygotic isolation barriers, so called (Bateson-)Dobzhansky-Muller incompatibilities or DMIs, among populations that are connected by gene flow. Specifically, we compare the relative stability of pairwise DMIs among autosomes, X chromosomes, and mitochondrial genes. In an analytical approach based on a continent-island framework, we determine how the maximum permissible migration rates depend on the genomic architecture of the DMI, on sex bias in migration rates, and on sex-dependence of allelic and epistatic effects, such as dosage compensation. Our results show that X-linkage of DMIs can enlarge the migration bounds relative to autosomal DMIs or autosome-mitochondrial DMIs, in particular in the presence of dosage compensation. The effect is further strengthened with male-biased migration. This mechanism might contribute to a higher density of DMIs on the X chromosome (large X-effect) that has been observed in sever...
Genetic tradeoff as a model for parapatric speciation
This paper uses an individual-based modelling approach to explore the effects of genetic tradeoff across a spatial gradient. Tradeoff is represented by the ability of an individual to live at higher environmental values-individuals that can live at high values can also live at low values, but the cost for this generalised ability is an increased time to breeding maturity. This paper shows that for very low tradeoff gradients significant zones still occur across the environment, with a pronounced set of heterozygotic bands. It is proposed that these bands represent hybrid zones, and that the model demonstrates that weak tradeoff across an environmental gradient can produce isolated genetic individuals. This model therefore shows one mechanism leading to parapatric speciation.
Speciation as a positive feedback loop between postzygotic and prezygotic barriers to gene flow
Proceedings of The Royal Society B: Biological Sciences, 2003
Speciation is intimately associated with the evolution of sex-and-reproduction-related traits, including those affecting hybrid incompatibility (postzygotic isolation) and species recognition (prezygotic isolation). Genes controlling such traits are not randomly distributed in the genome but are particularly abundant on the sex chromosomes. However, the evolutionary consequences of the sex linkage of genes involved in speciation have been little explored. Here, we present simulations of a continent-island diploid model that examines the effects of reduced recombination using both autosomal and sex-linked inheritance. We show first that linkage between genes affecting postzygotic and prezygotic isolation leads to a positive feedback loop in which both are strengthened. As species recognition evolves, genes causing hybrid incompatibility will hitchhike along with those improving premating isolation, leading to stronger hybrid incompatibility and thus increased pressure for further preference divergence. Second, we show that this loop effect is generally enhanced by sex linkage, because recombination is eliminated in the heterogametic sex, leading to tighter effective linkage between the two classes of genes and because natural selection is more efficient at sex-linked loci, as recessive alleles are not masked by dominance in the heterogametic sex. Accordingly, hitchhiking can be important in promoting speciation and can also lead to increased postzygotic isolation through adaptive evolution.
Speciation in peripheral populations: effects of drift load and mating systems
Journal of Evolutionary Biology, 2016
Speciation in peripheral populations has long been considered one of the most plausible scenarios for speciation with gene flow. In this study, however we identify two additional problems of peripatric speciation, as compared to the parapatric case, that may impede the completion of the speciation process for most parameter regions. First, with (predominantly) unidirectional gene flow, there is no selection pressure to evolve assortative mating on the continent. We discuss the implications of this for different mating schemes. Second, genetic load can build up in small populations. This can lead to extinction of the peripheral species, or generate selection pressure for lower assortative mating to avoid inbreeding. In this case, either a stable equilibrium with intermediate assortment evolves or there is cycling between phases of hybridization and phases of complete isolation.
Speciation with gene flow on Lord Howe Island
Understanding the processes underlying the origin of species is a fundamental goal of biology. It is widely accepted that speciation requires an interruption of gene flow between populations: Ongoing gene exchange is considered a major hindrance to population divergence and, ultimately, to the evolution of new species. Where a geographic barrier to reproductive isolation is lacking, a biological mechanism for speciation is required to counterbalance the homogenizing effect of gene flow. Speciation with initially strong gene flow is thought to be extremely rare, and few convincing empirical examples have been published. However, using phylogenetic, karyological, and ecological data for the flora of a minute oceanic island (Lord Howe Island, LHI), we demonstrate that speciation with gene flow may, in fact, be frequent in some instances and could account for one in five of the endemic plant species of LHI. We present 11 potential instances of species divergence with gene flow, including an in situ radiation of five species of Coprosma (Rubiaceae, the coffee family). These results, together with the speciation of Howea palms on LHI, challenge current views on the origin of species diversity.
The effects of linkage and gene flow on local adaptation: A two-locus continent–island model
Theoretical Population Biology, 2011
Population subdivision and migration are generally considered to be important causes of linkage disequilibrium (LD). We explore the combined effects of recombination and gene flow on the amount of LD, the maintenance of polymorphism, and the degree of local adaptation in a subdivided population by analyzing a diploid, deterministic continent-island model with genic selection on two linked loci (i.e., no dominance or epistasis). For this simple model, we characterize explicitly all possible equilibrium configurations. Simple and intuitive approximations for many quantities of interest are obtained in limiting cases, such as weak migration, weak selection, weak or strong recombination. For instance, we derive explicit expressions for the measures D (= p AB − p A p B ) and r 2 (the squared correlation in allelic state) of LD. They depend in qualitatively different ways on the migration rate. Remarkably high values of r 2 are maintained between weakly linked loci, especially if gene flow is low. We determine how the maximum amount of gene flow that admits preservation of the locally adapted haplotype, hence of polymorphism at both loci, depends on recombination rate and selection coefficients. We also investigate the evolution of differentiation by examining the invasion of beneficial mutants of small effect that are linked to an already present, locally adapted allele. Mutants of much smaller effect can invade successfully than predicted by naive single-locus theory provided they are at least weakly linked. Finally, the influence of linkage on the degree of local adaptation, the migration load, and the effective migration rate at a neutral locus is explored. We discuss possible consequences for the evolution of genetic architecture, in particular, for the emergence of clusters of tightly linked, slightly beneficial mutations and the evolution of recombination and chromosome inversions.
Emergent speciation by multiple Dobzhansky-Muller incompatibilities
2014
The Dobzhansky-Muller model posits that incompatibilities between alleles at different loci cause speciation. However, it is known that if the alleles involved in a Dobzhansky-Muller incompatibility (DMI) between two loci are neutral, the resulting reproductive isolation cannot be maintained in the presence of either mutation or gene flow. Here we show that speciation can emerge through the collective effects of multiple neutral DMIs that cannot, individually, cause speciation-a mechanism we call emergent speciation. We investigate emergent speciation using models of haploid holey adaptive landscapes-neutral networks-with recombination. We find that certain combinations of multiple neutral DMIs can lead to speciation. Furthermore, emergent speciation is a robust mechanism that can occur in the presence of migration, and of deviations from the assumptions of the neutral network model. Strong recombination and complex interactions between the DMI loci facilitate emergent speciation. T...
PLoS Computational Biology, 2008
A commonly held view in evolutionary biology is that speciation (the emergence of genetically distinct and reproductively incompatible subpopulations) is driven by external environmental constraints, such as localized barriers to dispersal or habitat-based variation in selection pressures. We have developed a spatially explicit model of a biological population to study the emergence of spatial and temporal patterns of genetic diversity in the absence of predetermined subpopulation boundaries. We propose a 2-D cellular automata model showing that an initially homogeneous population might spontaneously subdivide into reproductively incompatible species through sheer isolation-by-distance when the viability of offspring decreases as the genomes of parental gametes become increasingly different. This simple implementation of the Dobzhansky-Muller model provides the basis for assessing the process and completion of speciation, which is deemed to occur when there is complete postzygotic isolation between two subpopulations. The model shows an inherent tendency toward spatial self-organization, as has been the case with other spatially explicit models of evolution. A well-mixed version of the model exhibits a relatively stable and unimodal distribution of genetic differences as has been shown with previous models. A much more interesting pattern of temporal waves, however, emerges when the dispersal of individuals is limited to short distances. Each wave represents a subset of comparisons between members of emergent subpopulations diverging from one another, and a subset of these divergences proceeds to the point of speciation. The long-term persistence of diverging subpopulations is the essence of speciation in biological populations, so the rhythmic diversity waves that we have observed suggest an inherent disposition for a population experiencing isolation-by-distance to generate new species.