Mechanisms of reinforcement in natural and simulated polymorphic populations

Reinforcement speciation is the process whereby selection against hybrids drives the evolution of enhanced pre-mating reproductive isolation. Work has focused on divergent mating preferences (assortative mating) but pre-mating isolation can also arise via various migration modification behaviours, such as divergent habitat preferences. The relative importance of these two different mechanisms of reinforcement remains unclear. A recent theoretical model (Yukilevich-True model) found that relative fixation probabilities between these mechanisms can vary. Additionally, natural populations of Timema cristinae walking-sticks exhibit variation (polymorphism) in both mechanisms, generating questions about the patterns expected for allele frequencies prior to fixation, during the early stages of the speciation process. In the present study, we report: (1) new analyses examining the correlation between fixation probabilities for assortative mating and migration modification in the Yukilevich-True model; (2) novel simulations examining allele frequencies in polymorphic populations; and (3) empirical patterns of reinforcement in T. cristinae in the context of theoretical predictions. Simulations of both types yielded congruent results, revealing that the outcome of reinforcement was dependent on the strength of selection. Under weak selection, reinforcement by either mechanism is unlikely. Under intermediate selection, the conditions favoring the rise and fixation of one mechanism favored the rise and fixation of the other. However, assortative mating evolved somewhat more readily than migration modification. Populations of T. cristinae, which experience such intermediate selection, supported these predictions. Under strong selection, the evolution of migration modification generally interfered with the evolution of assortative mating by decreasing migration between populations, thereby reducing selection for assortative mating. Congruence of the results for allele frequencies versus fixation probabilities suggests that similar patterns of reinforcement are expected during different stages of the speciation process

Increasing Our Ability to Predict Contemporary Evolution

Classic debates concerning the extent to which scientists can predict evolution have gained new urgency as environmental changes force species to adapt or risk extinction. We highlight how our ability to predict evolution can be constrained by data limitations that cause poor understanding of deterministic natural selection. We then emphasize how such data limits can be reduced with feasible empirical effort involving a combination of approaches

Evolution of Camouflage Drives Rapid Ecological Change in an Insect Community

SummaryBackgroundEvolutionary change in individual species has been hypothesized to have far-reaching consequences for entire ecological communities [1–3], and such coupling of ecological and evolutionary dynamics (“eco-evolutionary dynamics”) has been demonstrated for a variety systems [4–7]. However, the general importance of evolutionary dynamics for ecological dynamics remains unclear. Here, we investigate how spatial patterns of local adaptation in the stick insect Timema cristinae, driven by the interaction between multiple evolutionary processes, structure metapopulations, communities, and multitrophic interactions.ResultsObservations of a wild T. cristinae metapopulation show that locally imperfect camouflage reduces population size and that the effect of such maladaptation is comparable to the effects of more traditional ecological factors, including habitat patch size and host-plant species identity. Field manipulations of local adaptation and bird predation support the hypothesis that maladaptation reduces population size through an increase in bird predation. Furthermore, these field experiments show that maladaptation in T. cristinae and consequent increase in bird predation reduce the pooled abundance and species richness of the co-occurring arthropod community, and ultimately cascade to decrease herbivory on host plants. An eco-evolutionary model of the observational data demonstrates that the demographic cost of maladaptation decreases habitat patch occupancy by T. cristinae but enhances metapopulation-level adaptation.ConclusionsThe results demonstrate a pervasive effect of ongoing evolution in a spatial context on population and community dynamics. The eco-evolutionary model makes testable predictions about the influence of the spatial configuration of the patch network on metapopulation size and the spatial scale of adaptation

Observational evidence that maladaptive gene flow reduces patch occupancy in a wild insect metapopulation: BRIEF COMMUNICATION

Theory predicts that dispersal throughout metapopulations has a variety of consequences for the abundance and distribution of species. Immigration is predicted to increase abundance and habitat patch occupancy, but gene flow can have both positive and negative demographic consequences. Here, we address the eco-evolutionary effects of dispersal in a wild metapopulation of the stick insect Timema cristinae, which exhibits variable degrees of local adaptation throughout a heterogeneous habitat patch network of two host-plant species. To disentangle the ecological and evolutionary contributions of dispersal to habitat patch occupancy and abundance, we contrasted the effects of connectivity to populations inhabiting conspecific host plants and those inhabiting the alternate host plant. Both types of connectivity should increase patch occupancy and abundance through increased immigration and sharing of beneficial alleles through gene flow. However, connectivity to populations inhabiting the alternate host-plant species may uniquely cause maladaptive gene flow that counters the positive demographic effects of immigration. Supporting these predictions, we find the relationship between patch occupancy and alternate-host connectivity to be significantly smaller in slope than the relationship between patch occupancy and conspecific-host connectivity. Our findings illustrate the ecological and evolutionary roles of dispersal in driving the distribution and abundance of species

Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow

Theory predicts that speciation-with-gene-flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome-wide impacts of host-associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation-with-gene-flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co-occurring apple and hawthorn flies in nature. This striking genome-wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco-evolutionary dynamics and genome divergence

Ecological Niche Dimensionality and the Evolutionary Diversification of Stick Insects

The degree of phenotypic divergence and reproductive isolation between taxon pairs can vary quantitatively, and often increases as evolutionary divergence proceeds through various stages, from polymorphism to population differentiation, ecotype and race formation, speciation, and post-speciational divergence. Although divergent natural selection promotes divergence, it does not always result in strong differentiation. For example, divergent selection can fail to complete speciation, and distinct species pairs sometimes collapse (‘speciation in reverse’). Widely-discussed explanations for this variability concern genetic architecture, and the geographic arrangement of populations. A less-explored possibility is that the degree of phenotypic and reproductive divergence between taxon pairs is positively related to the number of ecological niche dimensions (i.e., traits) subject to divergent selection. Some data supporting this idea stem from laboratory experimental evolution studies using Drosophila, but tests from nature are lacking. Here we report results from manipulative field experiments in natural populations of herbivorous Timema stick insects that are consistent with this ‘niche dimensionality’ hypothesis. In such insects, divergent selection between host plants might occur for cryptic colouration (camouflage to evade visual predation), physiology (to detoxify plant chemicals), or both of these niche dimensions. We show that divergent selection on the single niche dimension of cryptic colouration can result in ecotype formation and intermediate levels of phenotypic and reproductive divergence between populations feeding on different hosts. However, greater divergence between a species pair involved divergent selection on both niche dimensions. Although further replication of the trends reported here is required, the results suggest that dimensionality of selection may complement genetic and geographic explanations for the degree of diversification in nature

Genome-Wide Association Mapping of Phenotypic Traits Subject to a Range of Intensities of Natural Selection in Timema cristinae*

abstract: The genetic architecture of adaptive traits can reflect the evolutionary history of populations and also shape divergence among populations. Despite this central role in evolution, relatively little is known regarding the genetic architecture of adaptive traits in nature, particularly for traits subject to known selection intensities. Here we quantitatively describe the genetic architecture of traits that are subject to known intensities of differential selection between host plant species in Timema cristinae stick insects. Specifically, we used phenotypic measurements of 10 traits and 211,004 single-nucleotide polymorphisms (SNPs) to conduct multilocus genome-wide association mapping. We identified a modest number of SNPs that were associated with traits and sometimes explained a large proportion of trait variation. These SNPs varied in their strength of association with traits, and both major and minor effect loci were discovered. However, we found no relationship between variation in levels of divergence among traits in nature and variation in parameters describing the genetic architecture of those same traits. Our results provide a first step toward identifying loci underlying adaptation in T. cristinae. Future studies will examine the genomic location, population differentiation, and response to selection of the trait-associated SNPs described here

Genome-wide differentiation in closely related populations: the roles of selection and geographic isolation.

Population divergence in geographic isolation is due to a combination of factors. Natural and sexual selection may be important in shaping patterns of population differentiation, a pattern referred to as 'Isolation by Adaptation' (IBA). IBA can be complementary to the well-known pattern of 'Isolation by Distance' (IBD), in which the divergence of closely related populations (via any evolutionary process) is associated with geographic isolation. The barn swallow Hirundo rustica complex comprises six closely related subspecies, where divergent sexual selection is associated with phenotypic differentiation among allopatric populations. To investigate the relative contributions of selection and geographic distance to genome-wide differentiation, we compared genotypic and phenotypic variation from 350 barn swallows sampled across eight populations (28 pairwise comparisons) from four different subspecies. We report a draft whole genome sequence for H. rustica, to which we aligned a set of 9,493 single nucleotide polymorphisms (SNPs). Using statistical approaches to control for spatial autocorrelation of phenotypic variables and geographic distance, we find that divergence in traits related to migratory behavior and sexual signaling, as well as geographic distance together, explain over 70% of genome-wide divergence among populations. Controlling for IBD, we find 42% of genome-wide divergence is attributable to IBA through pairwise differences in traits related to migratory behavior and sexual signaling alone. By (i) combining these results with prior studies of how selection shapes morphological differentiation and (ii) accounting for spatial autocorrelation, we infer that morphological adaptation plays a large role in shaping population-level differentiation in this group of closely related populations. This article is protected by copyright. All rights reserved

Lateral transfers of large DNA fragments spread functional genes among grasses

A fundamental tenet of multicellular eukaryotic evolution is that vertical inheritance is paramount, with natural selection acting on genetic variants transferred from parents to offspring. This lineal process means that an organism's adaptive potential can be restricted by its evolutionary history, the amount of standing genetic variation, and its mutation rate. Lateral gene transfer (LGT) theoretically provides a mechanism to bypass many of these limitations, but the evolutionary importance and frequency of this process in multicellular eukaryotes, such as plants, remains debated. We address this issue by assembling a chromosome-level genome for the grass Alloteropsis semialata, a species surmised to exhibit two LGTs, and screen it for other grass-to-grass LGTs using genomic data from 146 other grass species. Through stringent phylogenomic analyses, we discovered 57 additional LGTs in the A. semialata nuclear genome, involving at least nine different donor species. The LGTs are clustered in 23 laterally acquired genomic fragments that are up to 170 kb long and have accumulated during the diversification of Alloteropsis. The majority of the 59 LGTs in A. semialata are expressed, and we show that they have added functions to the recipient genome. Functional LGTs were further detected in the genomes of five other grass species, demonstrating that this process is likely widespread in this globally important group of plants. LGT therefore appears to represent a potent evolutionary force capable of spreading functional genes among distantly related grass species

Divergent host-plant adaptation and the evolution of reproductive isolation

Understanding the process of speciation requires elucidating the processes driving and constraining the evolution of reproductive isolation. For example, reproductive isolation can evolve simply as a by-product of populations adapting to different ecological environments. This process of ‘ecological speciation’ predicts greater levels of reproductive isolation between ecologically-divergent pairs of populations than between ecologically-similar pairs of similar age. The evolution of reproductive isolation can also be promoted by selection against hybrids (reinforcement) and can be constrained by the homogenizing effects of gene flow. This the sis examines the role of selection and gene flow in the evolution of reproductive isolation among host-associated populations of Timema cristinae walking-stick insects. Populations living on different host-plant species (Ceanothus versus Adenostoma) exhibit genetically-based, adaptive divergence in a suite of traits, including color, color-pattern, body size, body shape and behavior. Multiple forms of reproductive isolation were greater between populations using different hosts than between similar-aged populations using the same host. This pattern was detected for habitat isolation, immigrant inviability, sexual isolation, and cryptic postmating isolation, indicating that divergent host-plant adaptation promoted the evolution of multiple reproductive barriers. Conversely, gene flow between populations tended to erode divergence, with the exception of sexual isolation where moderate levels of gene flow promoted reinforcement. Molecular and morphological evidence suggest that the host-associated forms of T. cristinae are unlikely to have achieved species status such that the host forms represent either an ongoing speciation event or population divergence that has reached equilibrium. Studies of more divergent taxa in the genus are required to build up a more complete understanding of how the process of speciation unfolds, from beginning to end