Reinforcement’s incidental effects on reproductive isolation between conspecifics

Reinforcement—the process whereby maladaptive hybridization leads to the strengthening of prezygotic isolation between species—has a long history in the study of speciation. Because reinforcement affects traits involved in mate choice and fertility, it can have indirect effects on reproductive isolation between populations within species. Here we review examples of these “cascading effects of reinforcement” (CER) and discuss different mechanisms through which they can arise. We discuss three factors that are predicted to influence the potential occurrence of CER: rates of gene flow among populations, the strength of selection acting on the traits involved in reinforcement, and the genetic basis of those traits. We suggest that CER is likely if (1) the rate of gene flow between conspecific populations is low; (2) divergent selection acts on phenotypes involved in reinforcement between sympatric and allopatric populations; and (3) the genetic response to reinforcement differs among conspecific populations subject to parallel reinforcing selection. Future work continuing to address gene flow, selection, and the genetic basis of the traits involved in the reinforcement will help develop a better understanding of reinforcement as a process driving the production of species diversity, both directly and incidentally

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement in Drosophila yakuba

Selection against maladaptive hybridization can drive the evolution of reproductive isolation in a process called reinforcement. While the importance of reinforcement in evolution has been historically debated, many examples now exist. Despite these examples, we typically lack a detailed understanding of the mechanisms limiting the spread of reinforced phenotypes throughout a species' range. Here we address this issue in the fruit fly Drosophila yakuba, a species that hybridizes with its sister species D. santomea and is undergoing reinforcement in a well-defined hybrid zone on the island of São Tomé. Within this region, female D. yakuba show increased postmating-prezygotic (gametic) isolation towards D. santomea when compared with females from allopatric populations. We use a combination of natural collections, fertility assays, and experimental evolution to understand why reinforced gametic isolation in D. yakuba is confined to this hybrid zone. We show that, among other traits, D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results provide a novel example of reinforcement acting on a postmating-prezygotic trait in males, resulting in a cascade of reproductive isolation among conspecific populations

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement in Drosophila yakuba

Selection against maladaptive hybridization can drive the evolution of reproductive isolation in a process called reinforcement. While the importance of reinforcement in evolution has been historically debated, many examples now exist. Despite these examples, we typically lack a detailed understanding of the mechanisms limiting the spread of reinforced phenotypes throughout a species' range. Here we address this issue in the fruit fly Drosophila yakuba, a species that hybridizes with its sister species D. santomea and is undergoing reinforcement in a well-defined hybrid zone on the island of São Tomé. Within this region, female D. yakuba show increased postmating-prezygotic (gametic) isolation towards D. santomea when compared with females from allopatric populations. We use a combination of natural collections, fertility assays, and experimental evolution to understand why reinforced gametic isolation in D. yakuba is confined to this hybrid zone. We show that, among other traits, D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results provide a novel example of reinforcement acting on a postmating-prezygotic trait in males, resulting in a cascade of reproductive isolation among conspecific populations

Genomic signatures of admixture and selection are shared among populations of <i>Zaprionus indianus</i> across the western hemisphere

Introduced species have become an increasingly common component of biological communities around the world. A central goal in invasion biology is therefore to identify the demographic and evolutionary factors that underlie successful introductions. Here we use whole genome sequences, collected from populations in the native and introduced range of the African fig fly, Zaprionus indianus, to quantify genetic relationships among them, identify potential sources of the introductions, and test for selection at different spatial scales. We find that geographically widespread populations in the western hemisphere are genetically more similar to each other than to lineages sampled across Africa, and that these populations share a mixture of alleles derived from differentiated African lineages. Using patterns of allele‐sharing and demographic modelling we show that Z. indinaus have undergone a single expansion across the western hemisphere with admixture between African lineages predating this expansion. We also find support for selection that is shared across populations in the western hemisphere, and in some cases, with a subset of African populations. This suggests either that parallel selection has acted across a large part of Z. indianus's introduced range; or, more parsimoniously, that Z. indianus has experienced selection early on during (or prior‐to) its expansion into the western hemisphere. We suggest that the range expansion of Z. indianus has been facilitated by admixture and selection, and that management of this invasion could focus on minimizing future admixture by controlling the movement of individuals within this region rather than between the western and eastern hemisphere

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

Genetic diversity and thermal performance in invasive and native populations of African fig flies

During biological invasions, invasive populations can suffer losses of genetic diversity that are predicted to negatively impact their fitness/performance. Despite examples of invasive populations harboring lower diversity than conspecific populations in their native range, few studies have linked this lower diversity to a decrease in fitness. Using genome sequences, we show that invasive populations of the African fig fly, Zaprionus indianus, have less genetic diversity than conspecific populations in their native range and that diversity is proportionally lower in regions of the genome experiencing low recombination rates. This result suggests that selection may have played a role in lowering diversity in the invasive populations. We next use interspecific comparisons to show that genetic diversity remains relatively high in invasive populations of Z. indianus when compared to other closely related species. By comparing genetic diversity in orthologous gene regions, we also show that the genome-wide landscape of genetic diversity differs between invasive and native populations of Z. indianus, indicating that invasion not only affects amounts of genetic diversity, but also how that diversity is distributed across the genome. Finally, we use parameter estimates from thermal performance curves measured for 13 species of Zaprionus to show that Z. indianus has the broadest thermal niche of measured species, and that performance does not differ between invasive and native populations. These results illustrate how aspects of genetic diversity in invasive species can be decoupled from measures of fitness, and that a broad thermal niche may have helped facilitate Z. indianus's range expansion.Funding provided by: National Science FoundationCrossref Funder Registry ID: http://dx.doi.org/10.13039/100000001Award Number: Dimensions of Biodiversity award number 1737752Data used to generate genome annotations was generated by extracting whole RNA from groups of ~5 adult flies (24 hours after eclosion). Transcripts were assembed using Trinity (Grabherr et al. 2011; Hass et al. 2013) and annotations were generated using the MAKER pipeline (v3.01.02; Holt and Yandell 2011; Campbell et al. 2014). Data on thermal performance we generated in the lab under controlled conditions. All scripts used to fit thermal performance curves are given in this Dryad deposit. Software available for the method used are available at github.com/silastittes/performr

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

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

Highly Contiguous Assemblies of 101 Drosophilid Genomes

Over 100 years of studies in Drosophila melanogaster and related species in the genus Drosophila have facilitated key discoveries in genetics, genomics, and evolution. While high-quality genome assemblies exist for several species in this group, they only encompass a small fraction of the genus. Recent advances in long-read sequencing allow high-quality genome assemblies for tens or even hundreds of species to be efficiently generated. Here, we utilize Oxford Nanopore sequencing to build an open community resource of genome assemblies for 101 lines of 93 drosophilid species encompassing 14 species groups and 35 sub-groups. The genomes are highly contiguous and complete, with an average contig N50 of 10.5 Mb and greater than 97% BUSCO completeness in 97/101 assemblies. We show that Nanopore-based assemblies are highly accurate in coding regions, particularly with respect to coding insertions and deletions. These assemblies, along with a detailed laboratory protocol and assembly pipelines, are released as a public resource and will serve as a starting point for addressing broad questions of genetics, ecology, and evolution at the scale of hundreds of species