Accumulation Of Reproductive Isolation Research Articles

RAD-sequencing reveals patterns of diversification and hybridization, and the accumulation of reproductive isolation in a clade of partially sympatric, tropical island trees.

A common pattern observed in temperate tree clades is that species are often morphologically distinct and partially interfertile but maintain species cohesion despite ongoing hybridization where ranges overlap. Although closely related species commonly occur in sympatry in tropical ecosystems, little is known about patterns of hybridization within a clade over time, and the implications of this hybridization for the maintenance of species boundaries. In this study, we focused on a clade of sympatric trees in the genus Diospyros in the Mascarene islands and investigated whether species are genetically distinct, whether they hybridize, and how patterns of hybridization are related to the time since divergence among species. We sampled multiple populations from each of 12 Mascarene Diospyros species, generated genome-wide single nucleotide polymorphism data using 2bRADseq, and conducted population genomic and phylogenomic analyses. We found that Mascarene Diospyros species diverged millions of years ago and are today largely genetically distinct from one another. Although hybridization was observed between closely related species belonging to the same subclade, more distantly related species showed little evidence of interspecific hybridization. Phylogenomic analyses also suggested that introgression has occurred during the evolutionary history of the clade. This suggests that, as diversification progressed, interspecific hybridization occurred among species, but became infrequent as lineages diverged from one another and evolved reproductive barriers. Species now coexist in partial sympatry, and experience limited hybridization between close relatives. Additional research is needed to better understand the role that introgression may have played in adaptation and diversification of Mascarene Diospyros, and its relevance for conservation.

Genetic and chemical divergence among host races of a socially parasitic ant.

Host–parasite associations facilitate the action of reciprocal selection and can drive rapid evolutionary change. When multiple host species are available to a single parasite, parallel specialization on different hosts may promote the action of diversifying natural selection and divergence via host race formation. Here, we examine a population of the kidnapper ant (Polyergus mexicanus) that is an obligate social parasite of three sympatric ant species: Formica accreta, F. argentea, and F. subaenescens (formerly F. fusca). Behavioral and ecological observations of P. mexicanus have shown that individual colonies parasitize only one species of host and that new Polyergus queens maintain host fidelity when establishing new colonies. To successfully adapt to a particular host, Polyergus ants may mimic or camouflage themselves with the species‐specific chemical cues (cuticular hydrocarbons) that their hosts use to ascertain colony membership. To investigate the extent of host specialization, we collected both genetic and chemical data from P. mexicanus that parasitize each of the three different Formica species in sympatry. We show that host‐associated genetic structure exists for both maternally inherited mitochondrial DNA data and biparentally inherited microsatellite markers. We also show that P. mexicanus can be distinguished by chemical profile according to host due to partial matching with their host. Our results support the hypothesis that host race formation is occurring among lineages of P. mexicanus that use different Formica hosts. Thus, this system may represent a promising model for illuminating the early steps of divergence, accumulation of reproductive isolation, and speciation.

Admixture, evolution, and variation in reproductive isolation in the Boechera puberula clade

BackgroundHybridization is very common in plants, and the incorporation of new alleles into existing lineages (i.e. admixture) can blur species boundaries. However, admixture also has the potential to increase standing genetic variation. With new sequencing methods, we can now study admixture and reproductive isolation at a much finer scale than in the past. The genus Boechera is an extraordinary example of admixture, with over 400 hybrid derivates of varying ploidy levels. Yet, few studies have assessed admixture in this genus on a genomic scale.ResultsIn this study, we used Genotyping-by-Sequencing (GBS) to clarify the evolution of the Boechera puberula clade, whose six members are scattered across the western United States. We further assessed patterns of admixture and reproductive isolation within the group, including two additional species (B. stricta and B. retrofracta) that are widespread across North America. Based on 14,815 common genetic variants, we found evidence for some cases of hybridization. We find evidence of both recent and more ancient admixture, and that levels of admixture vary across species.ConclusionsWe present evidence for a monophyletic origin of the B. puberula group, and a split of B. puberula into two subspecies. Further, when inferring reproductive isolation on the basis of presence and absence of admixture, we found that the accumulation of reproductive isolation between species does not seem to occur linearly with time since divergence in this system. We discuss our results in the context of sexuality and asexuality in Boechera.

The accumulation of reproductive isolation in early stages of divergence supports a role for sexual selection.

Models of speciation by sexual selection propose that male-female coevolution leads to the rapid evolution of behavioural reproductive isolation. Here, we compare the strength of behavioural isolation to ecological isolation, gametic incompatibility and hybrid inviability in a group of dichromatic stream fishes. In addition, we examine whether any of these individual barriers, or a combined measure of total isolation, is predicted by body shape differences, male colour differences, environmental differences or genetic distance. Behavioural isolation reaches the highest values of any barrier and is significantly greater than ecological isolation. No individual reproductive barrier is associated with any of the predictor variables. However, marginally significant relationships between male colour and body shape differences with ecological and behavioural isolation are discussed. Differences in male colour and body shape predict total reproductive isolation between species; hierarchical partitioning of these two variables' effects suggests a stronger role for male colour differences. Together, these results suggest an important role for divergent sexual selection in darter speciation but raise new questions about the mechanisms of sexual selection at play and the role of male nuptial ornaments.

Parasites can cause selection against migrants following dispersal between environments

Summary 1. The potential for selection against migrants to promote population divergence and speciation is well established in theory, yet there has been relatively little empirical work that has explicitly considered selection against migrants as a form of reproductive barrier, and its importance in the accumulation of reproductive isolation between populations has been overlooked until recently. 2. Parasites often differ between environments and can be an important source of selection on hosts, yet their contribution to population divergence in general, and selection against migrants in particular, is poorly understood. 3. Selection against migrants might be reduced if organisms escape parasitism when they disperse (natural enemy release). Alternatively, parasites could increase selection against migrants if, when they disperse, organisms encounter parasites to which they are poorly adapted. 4. Here we test experimentally the contribution that parasites could make to selection against migrants in the adaptive radiation of three‐spined sticklebacks. These fish have repeatedly colonized freshwater environments from marine ones, and this has repeatedly lead to rapid speciation. 5. We use transplant experiments of lab‐raised fish to simulate dispersal, and antihelminthic treatment to show that ancestral‐type marine sticklebacks contract higher burdens of novel parasites when introduced to freshwater, than in saltwater, and suffer a growth cost as a direct result. 6. Susceptibility to parasites and their detrimental effect is less in derived, freshwater fish from evolutionarily young populations, possibly as a result of selection for resistance. 7. Our results support a role for parasites in selection against migrants and population diversification. They do not support the hypothesis of ‘natural enemy release’.

Perspective: models of speciation: what have we learned in 40 years?

Theoretical studies of speciation have been dominated by numerical simulations aiming to demonstrate that speciation in a certain scenario may occur. What is needed now is a shift in focus to identifying more general rules and patterns in the dynamics of speciation. The crucial step in achieving this goal is the development of simple and general dynamical models that can be studied not only numerically but analytically as well. I review some of the existing analytical results on speciation. I first show why the classical theories of speciation by peak shifts across adaptive valleys driven by random genetic drift run into trouble (and into what kind of trouble). Then I describe the Bateson-Dobzhansky-Muller (BDM) model of speciation that does not require overcoming selection. I describe exactly how the probability of speciation, the average waiting time to speciation, and the average duration of speciation depend on the mutation and migration rates, population size, and selection for local adaptation. The BDM model postulates a rather specific genetic architecture of reproductive isolation. I then show exactly why the genetic architecture required by the BDM model should be common in general. Next I consider the multilocus generalizations of the BDM model again concentrating on the qualitative characteristics of speciation such as the average waiting time to speciation and the average duration of speciation. Finally, I consider two models of sympatric speciation in which the conditions for sympatric speciation were found analytically. A number of important conclusions have emerged from analytical studies. Unless the population size is small and the adaptive valley is shallow, the waiting time to a stochastic transition between the adaptive peaks is extremely long. However, if transition does happen, it is very quick. Speciation can occur by mutation and random drift alone with no contribution from selection as different populations accumulate incompatible genes. The importance of mutations and drift in speciation is augmented by the general structure of adaptive landscapes. Speciation can be understood as the divergence along nearly neutral networks and holey adaptive landscapes (driven by mutation, drift, and selection for adaptation to a local biotic and/or abiotic environment) accompanied by the accumulation of reproductive isolation as a by-product. The waiting time to speciation driven by mutation and drift is typically very long. Selection for local adaptation (either acting directly on the loci underlying reproductive isolation via their pleiotropic effects or acting indirectly via establishing a genetic barrier to gene flow) can significantly decrease the waiting time to speciation. In the parapatric case the average actual duration of speciation is much shorter than the average waiting time to speciation. Speciation is expected to be triggered by changes in the environment. Once genetic changes underlying speciation start, they go to completion very rapidly. Sympatric speciation is possible if disruptive selection and/or assortativeness in mating are strong enough. Sympatric speciation is promoted if costs of being choosy are small (or absent) and if linkage between the loci experiencing disruptive selection and those controlling assortative mating is strong.

PERSPECTIVE: MODELS OF SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS?

Theoretical studies of speciation have been dominated by numerical simulations aiming to demonstrate that speciation in a certain scenario may occur. What is needed now is a shift in focus to identifying more general rules and patterns in the dynamics of speciation. The crucial step in achieving this goal is the development of simple and general dynamical models that can be studied not only numerically but analytically as well. I review some of the existing analytical results on speciation. I first show why the classical theories of speciation by peak shifts across adaptive valleys driven by random genetic drift run into trouble (and into what kind of trouble). Then I describe the Bateson-Dobzhansky-Muller (BDM) model of speciation that does not require overcoming selection. I describe exactly how the probability of speciation, the average waiting time to speciation, and the average duration of speciation depend on the mutation and migration rates, population size, and selection for local adaptation. The BDM model postulates a rather specific genetic architecture of reproductive isolation. I then show exactly why the genetic architecture required by the BDM model should be common in general. Next I consider the multilocus generalizations of the BDM model again concentrating on the qualitative characteristics of speciation such as the average waiting time to speciation and the average duration of speciation. Finally, I consider two models of sympatric speciation in which the conditions for sympatric speciation were found analytically. A number of important conclusions have emerged from analytical studies. Unless the population size is small and the adaptive valley is shallow, the waiting time to a stochastic transition between the adaptive peaks is extremely long. However, if transition does happen, it is very quick. Speciation can occur by mutation and random drift alone with no contribution from selection as different populations accumulate incompatible genes. The importance of mutations and drift in speciation is augmented by the general structure of adaptive landscapes. Speciation can be understood as the divergence along nearly neutral networks and holey adaptive landscapes (driven by mutation, drift, and selection for adaptation to a local biotic and/or abiotic environment) accompanied by the accumulation of reproductive isolation as a by-product. The waiting time to speciation driven by mutation and drift is typically very long. Selection for local adaptation (either acting directly on the loci underlying reproductive isolation via their pleiotropic effects or acting indirectly via establishing a genetic barrier to gene flow) can significantly decrease the waiting time to speciation. In the parapatric case the average actual duration of speciation is much shorter than the average waiting time to speciation. Speciation is expected to be triggered by changes in the environment. Once genetic changes underlying speciation start, they go to completion very rapidly. Sympatric speciation is possible if disruptive selection and/or assortativeness in mating are strong enough. Sympatric speciation is promoted if costs of being choosy are small (or absent) and if linkage between the loci experiencing disruptive selection and those controlling assortative mating is strong.

The evolution of reproductive isolation in spatially structured populations.

Recent models of speciation have incorporated population structure and migration into the classic model of speciation in which reproductive isolation arises as a by-product of divergence. In this paper, we expanded these models to explore the joint effects of migration and population subdivision on speciation in a spatially explicit context. The results of our simulation support previous results concerning the influence of population subdivision on the accumulation of reproductive isolation. The simulation also shows that speciation in subdivided populations occurs most rapidly when subpopulations are not strictly allopatric. These results counter the widespread notion that speciation is most likely to occur in allopatric populations and suggest that there are useful insights to be gained by incorporating increasingly realistic types of population structure into models of speciation.

THE EVOLUTION OF REPRODUCTIVE ISOLATION IN SPATIALLY STRUCTURED POPULATIONS

Recent models of speciation have incorporated population structure and migration into the classic model of speciation in which reproductive isolation arises as a by-product of divergence. In this paper, we expanded these models to explore the joint effects of migration and population subdivision on speciation in a spatially explicit context. The results of our simulation support previous results concerning the influence of population subdivision on the accumulation of reproductive isolation. The simulation also shows that speciation in subdivided populations occurs most rapidly when subpopulations are not strictly allopatric. These results counter the widespread notion that speciation is most likely to occur in allopatric populations and suggest that there are useful insights to be gained by incorporating increasingly realistic types of population structure into models of speciation.

Clusters of new identical mutants and the fate of underdominant mutations.

Given favorable environmental and demographic conditions, premeiotic clusters of identical mutations can produce a broad distribution of the initial frequency of underdominant alleles. Because of these clusters, new underdominant mutations may not necessarily be as rare in a population as previously assumed. The fixation of underdominant mutations, especially those with low heterozygous fitness, is increased when mutations appear in a cluster due to a genetic change that occurred before germline differentiation. Most restrictions on the fixation of underdominant mutations in a single population, such as strong genetic drift, weak selection against mutant heterozygotes, isolated population structure, inbreeding, meiotic drive, and selection in favor of mutant homozygotes can be relaxed or even dropped. Instead, the fate of strong underdominant mutations is determined mainly by ecological and genetic factors that affect the cluster size distribution of new premeiotic mutations. Accumulation of reproductive isolation by the fixation of underdominant mutations becomes more feasible with clusters, and mutation is not always the weakest force during this evolutionary process. The large mean and variance of reproductive success in many multicellular species make it possible that even underdominant mutations with very low heterozygous fitness could contribute substantially to reproductive isolation.