The evolution of conditional dispersal and reproductive isolation along environmental gradients

Dispersal modulates gene flow throughout a population's spatial range. Gene flow affects adaptation at local spatial scales, and consequently impacts the evolution of reproductive isolation. A recent theoretical investigation has demonstrated that local adaptation along an environmental gradient, facilitated by the evolution of limited dispersal, can lead to parapatric speciation even in the absence of assortative mating. This and other studies assumed unconditional dispersal, so individuals start dispersing without regard to local environmental conditions. However, many species disperse conditionally; their propensity to disperse is contingent upon environmental cues, such as the degree of local crowding or the availability of suitable mates. Here, we use an individual-based model in continuous space to investigate by numerical simulation the relationship between the evolution of threshold-based conditional dispersal and parapatric speciation driven by frequency-dependent competition along environmental gradients. We find that, as with unconditional dispersal, parapatric speciation occurs under a broad range of conditions when reproduction is asexual, and under a more restricted range of conditions when reproduction is sexual. In both the asexual and sexual cases, the evolution of conditional dispersal is strongly influenced by the slope of the environmental gradient: shallow environmental gradients result in low dispersal thresholds and high dispersal distances, while steep environmental gradients result in high dispersal thresholds and low dispersal distances. The latter, however, remain higher than under unconditional dispersal, thus undermining isolation by distance, and hindering speciation in sexual populations. Consequently, the speciation of sexual populations under conditional dispersal is triggered by a steeper gradient than under unconditional dispersal. Enhancing the disruptiveness of frequency-dependent selection, more box-shaped competition kernels dramatically lower the speciation-enabling slope of the environmental gradient.     

Integrating GIS-based environmental data into evolutionary biology

Many evolutionary processes are influenced by environmental variation over space and time, including genetic divergence among populations, speciation and evolutionary change in morphology, physiology and behaviour. Yet, evolutionary biologists have generally not taken advantage of the extensive environmental data available from geographic information systems (GIS). For example, studies of phylogeography, speciation and character evolution often ignore or use only crude proxies for environmental variation (e.g. latitude and distance between populations). Here, we describe how the integration of GIS-based environmental data, along with new spatial tools, can transform evolutionary studies and reveal new insights into the ecological causes of evolutionary patterns.     

Does Sex Speed Up Evolutionary Rate and Increase Biodiversity?

Most empirical and theoretical studies have shown that sex increases the rate of evolution, although evidence of sex constraining genomic and epigenetic variation and slowing down evolution also exists. Faster rates with sex have been attributed to new gene combinations, removal of deleterious mutations, and adaptation to heterogeneous environments. Slower rates with sex have been attributed to removal of major genetic rearrangements, the cost of finding a mate, vulnerability to predation, and exposure to sexually transmitted diseases. Whether sex speeds or slows evolution, the connection between reproductive mode, the evolutionary rate, and species diversity remains largely unexplored. Here we present a spatially explicit model of ecological and evolutionary dynamics based on DNA sequence change to study the connection between mutation, speciation, and the resulting biodiversity in sexual and asexual populations. We show that faster speciation can decrease the abundance of newly formed species and thus decrease long-term biodiversity. In this way, sex can reduce diversity relative to asexual populations, because it leads to a higher rate of production of new species, but with lower abundances. Our results show that reproductive mode and the mechanisms underlying it can alter the link between mutation, evolutionary rate, speciation and biodiversity and we suggest that a high rate of evolution may not be required to yield high biodiversity.     

Will sympatric speciation fail due to stochastic competitive exclusion?

Sympatric speciation requires coexistence of the newly formed species. If divergence proceeds by small mutational steps, the new species utilize almost the same resources initially, and full speciation may be impeded by competitive exclusion in stochastic environments. We investigate this primarily ecological problem of sympatric speciation by studying the population dynamics of a diverging asexual population in a fluctuating environment. Correlation between species responses to environmental fluctuation is assumed to decrease with distance in trait space. Rapidly declining correlation in combination with high environmental variability may delay full speciation or even render it impossible. Stochastic extinctions impeding speciation are most likely when correlation decays faster than competition, for example, when demographic stochasticity is strong or when divergence is not accompanied by niche separation, such as in speciation driven entirely by sexual selection. Our general theoretical results show an interesting connection between short-term ecological dynamics and long-term, large-scale evolution.     

Poor male function favours the coexistence of sexual and asexual relatives

Classical models of the evolution of sex typically assume that an asexual lineage, once derived, is reproductively separate from the sexual lineage from which it was derived. However, many asexuals, including hermaphrodite plants, produce male gametes capable of fertilising the eggs of co-existing sexuals, giving rise to sexual and asexual progeny. This male function of asexuals may be poor, and it has been proposed that this could favour sexuality and adversely affect the successful establishment of asexual lineages. We show that things are more complicated than this; the effect is frequency-dependent and poor male function may sometimes favour asexuality. In a spatially distributed population of flowering plants, it can prevent the successful invasion of either reproductive mode by the other via long-range dispersal. Consequently invasions must be driven by short-range dispersal, and are therefore extremely slow. Thus poor male function favours long-term co-existence of sexuals and asexuals. When coupled with the superior ability of asexuals to colonise virgin territory after an Ice Age, it may explain current ecological distribution patterns.     

Signal Divergence is Correlated with Genetic Distance and not Environmental Differences in Darters (Percidae: Etheostoma)

Speciation research focuses on the evolutionary mechanisms responsible for the origin of species, and recent treatments have distinguished ecological and mutation-order speciation as distinct evolutionary processes. Using a research framework that considers ??speciation phenotypes?? (sensu Shaw and Mullen in Genet 139(5):649?C661, 2011) and a modified hierarchy of speciation models, we address whether speciation in benthic fishes commonly called darters proceeds under divergent ecological selection or a mutation-order process. We examined neutral genetic divergence, sexual signal (male color) divergence, environmental differences, and geographic distance in 66 species pair comparisons. Modified Mantel tests detected significant relationships between genetic distance and overall male color differences, as well as geographic distance and overall male color differences; however, after accounting for the correlation of male color and geographic distance with genetic distance using a partial Mantel test, no relationship was observed between male color and geographic distance. Neither microhabitat nor climatic measures of environmental differences correlated with overall male color differences. Color difference scores for discrete color categories (i.e., red/orange/yellow, black, and blue/green) differed in their correlations with explanatory variables, implying different selection regimes may be influencing each component of darter color patterns. Our results do not support a primary role for divergent ecological selection shaping early divergence of darter sexual signals. Instead, a model of mutation-order speciation may best explain the clock-like manner of changes in male color among darter species.     

Consequences of Dispersal Heterogeneity for Population Spread and Persistence

Dispersal heterogeneity is increasingly being observed in ecological populations and has long been suspected as an explanation for observations of non-Gaussian dispersal. Recent empirical and theoretical studies have begun to confirm this. Using an integro-difference model, we allow an individual’s diffusivity to be drawn from a trait distribution and derive a general relationship between the dispersal kernel’s moments and those of the underlying heterogeneous trait distribution. We show that dispersal heterogeneity causes dispersal kernels to appear leptokurtic, increases the population’s spread rate, and lowers the critical reproductive rate required for persistence in the face of advection. Wavespeed has been shown previously to be determined largely by the form of the dispersal kernel tail. We qualify this by showing that when reproduction is low, the precise shape of the tail is less important than the first few dispersal moments such as variance and kurtosis. If the reproductive rate is large, a dispersal kernel’s asymptotic tail has a greater influence over wavespeed, implying that estimating the prevalence of traits which correlate with long-range dispersal is critical. The presence of multiple dispersal behaviors has previously been characterized in terms of long-range versus short-range dispersal, and it has been found that rare long-range dispersal essentially determines wavespeed. We discuss this finding and place it within a general context of dispersal heterogeneity showing that the dispersal behavior with the highest average dispersal distance does not always determine wavespeed.     

Five questions on ecological speciation addressed with individual‐based simulations

We use an individual‐based simulation model to investigate factors influencing progress toward ecological speciation. We find that environmental differences can quickly lead to the evolution of substantial reproductive barriers between a population colonizing a new environment and the ancestral population in the old environment. Natural selection against immigrants and hybrids was a major contributor to this isolation, but the evolution of sexual preference was also important. Increasing dispersal had both positive and negative effects on population size in the new environment and had positive effects on natural selection against immigrants and hybrids. Genetic divergence at unlinked, neutral genetic markers was low, except when environmental differences were large and sexual preference was present. Our results highlight the importance of divergent selection and adaptive divergence for ecological speciation. At the same time, they reveal several interesting nonlinearities in interactions between environmental differences, sexual preference, dispersal and population size.     

Distance-dependent performance of asexual progeny in Allium vineale (Liliaceae)

Local adaptation within and among populations may have an impact on processes ranging from speciation to the evolution of mixed breeding systems and dispersal strategies. It is also one potential factor that could favor the production of asexual over sexual propagules. This field experiment tested whether asexually produced bulbils of Allium vineale demonstrate local adaptation to the parental microsite at the scale of natural dispersal from the parent (5, 25, 50, 100, and 1000 cm). Both "home' and randomly chosen "away' genotypes were planted at each location to determine the relative performance of the "home' genotype. Overall, bulbil performance declined with distance from the parent. In particular, "home' bulbils outperformed "away' bulbils at a distance of 25 cm from the parent, indicating that local adaptation has occurred at the scale of natural dispersal in this species. The variance in propagule performance also increased at farther distances from the parent, indicating that the predictability of offspring performance decreases with distance. Fine-scale local adaptation within the range of seed dispersal in this population may be one factor favoring asexual reproduction in Allium vineale.     

Loss of sexual recombination and segregation is associated with increased diversification in evening primroses

The loss of sexual recombination and segregation in asexual organisms has been portrayed as an irreversible process that commits asexually reproducing lineages to reduced diversification. We test this hypothesis by estimating rates of speciation, extinction, and transition between sexuality and functional asexuality in the evening primroses. Specifically, we estimate these rates using the recently developed BiSSE (Binary State Speciation and Extinction) phylogenetic comparative method, which employs maximum likelihood and Bayesian techniques. We infer that net diversification rates (speciation minus extinction) in functionally asexual evening primrose lineages are roughly eight times faster than diversification rates in sexual lineages, largely due to higher speciation rates in asexual lineages. We further reject the hypothesis that a loss of recombination and segregation is irreversible because the transition rate from functional asexuality to sexuality is significantly greater than zero and in fact exceeded the reverse rate. These results provide the first empirical evidence in support of the alternative theoretical prediction that asexual populations should instead diversify more rapidly than sexual populations because they are free from the homogenizing effects of sexual recombination and segregation. Although asexual reproduction may often constrain adaptive evolution, our results show that the loss of recombination and segregation need not be an evolutionary dead end in terms of diversification of lineages.     

Evolution of sexual systems, dispersal strategies and habitat selection in the liverwort genus Radula

? Shifts in sexual systems are among the most common and important transitions in plants and are correlated with a suite of life-history traits. The evolution of sexual systems and their relationships to gametophyte size, sexual and asexual reproduction, and epiphytism are examined here in the liverwort genus Radula. ? The sequence of trait acquisition and the phylogenetic correlations between those traits was investigated using comparative methods. ? Shifts in sexual systems recurrently occurred from dioecy to monoecy within facultative epiphyte lineages. Production of specialized asexual gemmae was correlated to neither dioecy nor strict epiphytism. ? The significant correlations among life-history traits related to sexual systems and habitat conditions suggest the existence of evolutionary trade-offs. Obligate epiphytes do not produce gemmae more frequently than facultative epiphytes and disperse by whole gametophyte fragments, presumably to avoid the sensitive protonemal stage in a habitat prone to rapid changes in moisture availability. As dispersal ranges correlate with diaspore size, this reinforces the notion that epiphytes experience strong dispersal limitations. Our results thus provide the evolutionary complement to metapopulation, metacommunity and experimental studies demonstrating trade-offs between dispersal distance, establishment ability, and life-history strategy, which may be central to the evolution of reproductive strategies in bryophytes.     

Population structure inhibits evolutionary diversification under competition for resources

A model is presented that explores how population structure affects the evolutionary outcome of ecological competition for resources. The model assumes that competition for resources occurs within groups of a finite number of individuals (interaction groups), and that limited dispersal of individuals between groups (according to Wright's island model of population structure) results in genetic structuring of the population. It is found that both finite-sized interaction groups and limited dispersal can have substantial effects on the evolution of resource exploitation strategies as compared to models with a single, infinitely large, well-mixed interaction group. Both effects, in general, tend to select for less aggressive competitive strategies. Moreover, both effects also tend to reduce the likelihood of the evolutionary diversification of resource exploitation strategies that often occurs in models of resource competition with infinite populations. The results are discussed in the context of theories of the evolutionary diversification of resource exploitation strategies and speciation.     

The effect of population size and recombination on delayed evolution of polymorphism and speciation in sexual populations

Recent theory suggests that absolute population size may qualitatively influence the outcome of evolution under disruptive selection in asexual populations. Large populations are predicted to undergo rapid evolutionary branching; however, in small populations, the waiting time to branching increases steeply with decreasing abundance, and below a critical size, the population remains monomorphic indefinitely. Here, we (1) extend the theory to sexual populations and (2) confront its predictions with empirical data, testing statistically whether lake size affects the level of resource polymorphism in arctic char (Salvelinus alpinus) in 22 lakes of different sizes. For a given level of recombination, our model predicts qualitatively similar relations between population size and time to evolutionary branching (either speciation or evolution of genetic polymorphism) as the asexual model, while recombination further increases the delay to branching. The loss of polymorphism at certain loci, an inherent aspect of multilocus-trait evolution, may increase the delay to speciation, resulting in stable genetic polymorphism without speciation. The empirical analysis demonstrates that the occurrence of resource polymorphism depends on both lake size and the number of coexisting fish species. For a given number of coexisting species, the level of polymorphism increases significantly with lake size, thus confirming our model prediction.     

The role of environment and core‐margin effects on range‐wide phenotypic variation in a montane grasshopper

The integration of genetic information with ecological and phenotypic data constitutes an effective approach to gain insight into the mechanisms determining interpopulation variability and the evolutionary processes underlying local adaptation and incipient speciation. Here, we use the Pyrenean Morales grasshopper (Chorthippus saulcyi moralesi) as study system to (i) analyse the relative role of genetic drift and selection in range‐wide patterns of phenotypic differentiation and (ii) identify the potential selective agents (environment, elevation) responsible for variation. We also test the hypothesis that (iii) the development of dispersal‐related traits is associated with different parameters related to population persistence/turnover, including habitat suitability stability over the last 120 000 years, distance to the species distribution core and population genetic variability. Our results indicate that selection shaped phenotypic differentiation across all the studied morphological traits (body size, forewing length and shape). Subsequent analyses revealed that among‐population differentiation in forewing length was significantly explained by a temperature gradient, suggesting an adaptive response to thermoregulation or flight performance under contrasting temperature regimes. We found support for our hypothesis predicting a positive association between the distance to the species distribution core and the development of dispersal‐related morphology, which suggests an increased dispersal capability in populations located at range edges that, in turn, exhibit lower levels of genetic variability. Overall, our results indicate that range‐wide patterns of phenotypic variation are partially explained by adaptation in response to local environmental conditions and differences in habitat persistence between core and peripheral populations.     

Adaptive Significance and Long-Term Survival of Asexual Lineages

Important questions remain about the long-term survival and adaptive significance of eukaryotic asexual lineages. Numerous papers dealing with sex advantages still continued to compare parthenogenetic populations versus sexual populations arguing that sex demonstrates a better fitness. Because asexual lineages do not possess any recombination mechanisms favoring rapid changes in the face of severe environmental conditions, they should be considered as an evolutionary dead-end. Nevertheless, reviewing literature dealing with asexual reproduction, it is possible to draw three stimulating conclusions. (1) Asexual reproduction in eukaryotes considerably differs from prokaryotes which experience recombination but neither meiosis nor syngamy. Recombination and meiosis would be a driving force for sexual reproduction. Eukaryotes should therefore be considered as a continuum of sexual organisms that are more or less capable (and sometimes incapable) of sexual reproduction. (2) Rather than revealing ancestral eukaryotic forms, most known lineages of asexual eukaryotes have lost sex due to a genomic conflict affecting their sexual capacity. Thus, it could be argued that hybridization is a major cause of their asexuality. Asexuality may have evolved as a reproductive mechanism reducing conflict within organisms. (3) It could be proposed that, rather than being generalists, parthenogenetic hybrid lineages could be favored when exploiting peculiar restricted ecological niches, following the “frozen niche variation” model. Although hybrid events may result in sex loss, probably caused by genomic conflict, asexual hybrids could display new original adaptive traits, and the rapid colonization of environments through clonal reproduction could favor their long-term survival, leading to evolutionary changes and hybrid speciation. Examination of the evolutionary history of asexual lineages reveals that evolutionary processes act through transitional stages in which even very small temporary benefits may be enough to counter the expected selective disadvantages.     

Replicate patterns of species richness, historical biogeography, and phylogeny in Holarctic treefrogs

In recent decades, the field of historical biogeography has become increasingly divorced from evolutionary biology, ecology, and studies of species richness. In this paper, we explore the evolutionary causes of patterns of biogeography and species richness in Northern Hemisphere treefrogs, combining phylogenetics, ancestral area reconstruction, molecular dating methods, and ecological niche modeling. We reconstructed phylogenetic relationships among 58 hylid taxa using data from two mitochondrial genes (12S, ND1) and two nuclear genes (POMC, c-myc). We find that parallel patterns of species richness have developed in Europe, Asia, and in two separate clades of North American hylids, with the highest richness at midtemperate latitudes (30-35 degrees) on each continent. This pattern is surprising given that hylids overall show higher species richness in the New World tropics and given many standard ecological explanations for the latitudinal diversity gradient (e.g., energy, productivity, mid-domain effect). The replicate pattern in Holarctic hylids seems to reflect specialized tolerance for temperate climate regimes or possibly the effects of competition. The results also suggest that long-range dispersal between continental regions with similar climatic regimes may be easier than dispersal between geographically adjacent regions with different climatic regimes. Our results show the importance of ecology and evolution to large-scale biogeography and the importance of large-scale biogeography to understanding patterns of species richness.     

The consequences of phenotypic plasticity for ecological speciation

We use an individual-based numerical simulation to study the effects of phenotypic plasticity on ecological speciation. We find that adaptive plasticity evolves readily in the presence of dispersal between populations from different ecological environments. This plasticity promotes the colonization of new environments but reduces genetic divergence between them. We also find that the evolution of plasticity can either enhance or degrade the potential for divergent selection to form reproductive barriers. Of particular importance here is the timing of plasticity in relation to the timing of dispersal. If plasticity is expressed after dispersal, reproductive barriers are generally weaker because plasticity allows migrants to be better suited for their new environment. If plasticity is expressed before dispersal, reproductive barriers are either unaffected or enhanced. Among the potential reproductive barriers we considered, natural selection against migrants was the most important, primarily because it was the earliest-acting barrier. Accordingly, plasticity had a much greater effect on natural selection against migrants than on sexual selection against migrants or on natural and sexual selection against hybrids. In general, phenotypic plasticity can strongly alter the process of ecological speciation and should be considered when studying the evolution of reproductive barriers.     

Parallel and nonparallel ecological,morphological and genetic divergence in lake–stream stickleback from a single catchment

Parallel phenotypic evolution in similar environments has been well studied in evolutionary biology; however, comparatively little is known about the influence of determinism and historical contingency on the nature, extent and generality of this divergence. Taking advantage of a novel system containing multiple lake–stream stickleback populations, we examined the extent of ecological, morphological and genetic divergence between three‐spined stickleback present in parapatric environments. Consistent with other lake–stream studies, we found a shift towards a deeper body and shorter gill rakers in stream fish. Morphological shifts were concurrent with changes in diet, indicated by both stable isotope and stomach contents analysis. Performing a multivariate test for shared and unique components of evolutionary response to the distance gradient from the lake, we found a strong signature of parallel adaptation. Nonparallel divergence was also present, attributable mainly to differences between river locations. We additionally found evidence of genetic substructuring across five lake–stream transitions, indicating that some level of reproductive isolation occurs between populations in these habitats. Strong correlations between pairwise measures of morphological, ecological and genetic distance between lake and stream populations supports the hypothesis that divergent natural selection between habitats drives adaptive divergence and reproductive isolation. Lake–stream stickleback divergence in Lough Neagh provides evidence for the deterministic role of selection and supports the hypothesis that parallel selection in similar environments may initiate parallel speciation.     

Inferring speciation modes in a clade of Iberian chafers from rates of morphological evolution in different character systems

Background  

Studies of speciation mode based on phylogenies usually test the predicted effect on diversification patterns or on geographical distribution of closely related species. Here we outline an approach to infer the prevalent speciation mode in Iberian Hymenoplia chafers through the comparison of the evolutionary rates of morphological character systems likely to be related to sexual or ecological selection. Assuming that mitochondrial evolution is neutral and not related to measured phenotypic differences among the species, we contrast hypothetic outcomes of three speciation modes: 1) geographic isolation with subsequent random morphological divergence, resulting in overall change proportional to the mtDNA rate; 2) sexual selection on size and shape of the male intromittent organs, resulting in an evolutionary rate decoupled to that of the mtDNA; and 3) ecological segregation, reflected in character systems presumably related to ecological or biological adaptations, with rates decoupled from that of the mtDNA.     

Junk DNA Contribution to Evolutionary Capacitance Can Drive Species Dynamics

Junk DNA is still an enigmatic concept. Although junk DNA composition, abundance, and functionality are still contentious, its contribution to biological evolution is less questionable. Recently, I proposed that sexually restricted chromosomes such as Y and W, highly enriched in junk DNA elements, act as genomic tuning knobs indirectly causing a genome-wide increase in gene expression heterogeneity that boosts heterogametic individuals ability to endure environmental challenges and evolutionary capacitance, i.e., the store of genetic variation with no phenotypic effect. Sexually restricted chromosomes-based evolutionary capacitance might importantly contribute to metazoan sexual dimorphisms for dispersal and sex-biased gene expression dynamics. In this Synthesis, I hypothesize that large differences between species in the overall amount of junk DNA within their genomes also promote differences in junk DNA-based evolutionary capacitance that might be reflected in differences for dispersal and genetic diversification. I hypothesize that populations for species with junk DNA-impoverished genomes would show an enhanced ability to genetically diversify leading to a faster speciation rate even in the absence of geographic isolation when compared with populations for species with junk DNA-enriched genomes. To support junk DNA variation-based evolutionary capacitance effect on species genetic diversification, I analyzed the covariation of genome size as proxy for the overall amount of junk DNA in the genome and several genetic diversification measures obtained from interspecific crosses for the Drosophilidae family. The potential effect of junk DNA variation-based evolutionary capacitance for other elements of species dynamics such as extinction or the participation in grouped ecological structures is also briefly discussed.