Showing papers by "Roger K. Butlin published in 2017"

Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow.

Abstract: Speciation, the evolution of reproductive isolation among populations, is continuous, complex, and involves multiple, interacting barriers. Until it is complete, the effects of this process vary along the genome and can lead to a heterogeneous genomic landscape with peaks and troughs of differentiation and divergence. When gene flow occurs during speciation, barriers restricting gene flow locally in the genome lead to patterns of heterogeneity. However, genomic heterogeneity can also be produced or modified by variation in factors such as background selection and selective sweeps, recombination and mutation rate variation, and heterogeneous gene density. Extracting the effects of gene flow, divergent selection and reproductive isolation from such modifying factors presents a major challenge to speciation genomics. We argue one of the principal aims of the field is to identify the barrier loci involved in limiting gene flow. We first summarize the expected signatures of selection at barrier loci, at the genomic regions linked to them and across the entire genome. We then discuss the modifying factors that complicate the interpretation of the observed genomic landscape. Finally, we end with a road map for future speciation research: a proposal for how to account for these modifying factors and to progress towards understanding the nature of barrier loci. Despite the difficulties of interpreting empirical data, we argue that the availability of promising technical and analytical methods will shed further light on the important roles that gene flow and divergent selection have in shaping the genomic landscape of speciation.

Coupling, reinforcement, and speciation

Abstract: During the process of speciation, populations may diverge for traits and at their underlying loci that contribute barriers to gene flow. These barrier traits and barrier loci underlie individual barrier effects, by which we mean the contribution that a barrier locus or trait—or some combination of barrier loci or traits—makes to overall isolation. The evolution of strong reproductive isolation typically requires the origin of multiple barrier effects. Critically, it also requires the coincidence of barrier effects; for example, two barrier effects, one due to assortative mating and the other due to hybrid inviability, create a stronger overall barrier to gene flow if they coincide than if they distinguish independent pairs of populations. Here, we define “coupling” as any process that generates coincidence of barrier effects, resulting in a stronger overall barrier to gene flow. We argue that speciation research, both empirical and theoretical, needs to consider both the origin of barrier effects ...

Local adaptation of reproductive performance during thermal stress

Abstract: Considerable evidence exists for local adaptation of critical thermal limits in ectotherms following adult temperature stress, but fewer studies have tested for local adaptation of sublethal heat stress effects across life-history stages. In organisms with complex life cycles, such as holometabolous insects, heat stress during juvenile stages may severely impact gametogenesis, having downstream consequences on reproductive performance that may be mediated by local adaptation, although this is rarely studied. Here, we tested how exposure to either benign or heat stress temperature during juvenile and adult stages, either independently or combined, influences egg-to-adult viability, adult sperm motility and fertility in high- and low-latitude populations of Drosophila subobscura. We found both population- and temperature-specific effects on survival and sperm motility; juvenile heat stress decreased survival and subsequent sperm motility and each trait was lower in the northern population. We found an interaction between population and temperature on fertility following application of juvenile heat stress; although fertility was negatively impacted in both populations, the southern population was less affected. When the adult stage was also subject to heat stress, the southern population exhibited positive carry-over effects whereas the northern population's fertility remained low. Thus, the northern population is more susceptible to sublethal reproductive consequences following exposure to juvenile heat stress. This may be common in other organisms with complex life cycles and current models predicting population responses to climate change, which do not take into account the impact of juvenile heat stress on reproductive performance, may be too conservative.

A genomic footprint of hybrid zone movement in crested newts

Abstract: Speciation typically involves a stage in which species can still exchange genetic material. Interspecific gene flow is facilitated by the hybrid zones that such species establish upon secondary contact. If one member of a hybridizing species pair displaces the other, their hybrid zone would move across the landscape. Although theory predicts that moving hybrid zones quickly stagnate, hybrid zones tracked over one or a few decades do not always follow such a limitation. This suggests that hybrid zones have the potential to traverse considerable distances over extended periods of time. When hybrid zones move, introgression is predicted to result in biased gene flow of selectively neutral alleles, from the receding species into the advancing species. We test for such a genomic footprint of hybrid zone movement in a pair of crested newt species (genus Triturus) for which we have a priori support for westward hybrid zone movement. We perform a multilocus phylogeographical survey and conduct Bayesian clustering analysis, estimation of ancestry and heterozygosity, and geographical cline analysis. In a 600 km wide area east of the present day hybrid zone a genomic footprint constitutes empirical evidence consistent with westward hybrid zone movement. The crested newt case suggests that hybrid zone movement can occur over an extensive span of time and space. Inferring hybrid zone movement provides fundamental insight into historical biogeography and the speciation process, and we anticipate that hybrid zones will prove to be far more mobile than currently appreciated.

A signature of dynamic biogeography: enclaves indicate past species replacement.

Abstract: Understanding how species have replaced each other in the past is important to predicting future species turnover. While past species replacement is difficult to detect after the fact, the process may be inferred from present-day distribution patterns. Species with abutting ranges sometimes show a characteristic distribution pattern, where a section of one species range is enveloped by that of the other. Such an enclave could indicate past species replacement: when a species is partly supplanted by a competitor, but a population endures locally while the invading species moves around and past it, an enclave forms. If the two species hybridize and backcross, the receding species is predicted to leave genetic traces within the expanding one under a scenario of species replacement. By screening dozens of genes in hybridizing crested newts, we uncover genetic remnants of the ancestral species, now inhabiting an enclave, in the range of the surrounding invading species. This independent genetic evidence supports the past distribution dynamics we predicted from the enclave. We suggest that enclaves provide a valuable tool in understanding historical species replacement, which is important because a major conservation concern arising from anthropogenic climate change is increased species replacement in the future.

Adaptation to dislodgement risk on wave-swept rocky shores in the snail Littorina saxatilis.

Abstract: The periwinkle Littorina saxatilis has repeatedly evolved both a small, fragile and globose "wave ecotype" confined to wave-swept shores and a large, robust and elongated "crab ecotype" found in nearby crab-rich but less-exposed shores. This phenotypic divergence is assumed to reflect, in some part, local adaptation to wave exposure, but this hypothesis has received incomplete experimental testing. Here, we report a test of the prediction that the wave ecotype has a higher capacity to resist water flow than the crab ecotype. We sampled snails along a crab-wave transect and measured their resistance to dislodgement in a high-speed water flume with water speeds that match those of breaking waves in a range of relevant field conditions. Snails from the wave environment were consistently more resistant to water flow than snails from the crab environment and high resistance was positively correlated with the surface area of the foot and the area of the outer aperture contour both relative to shell size, and to the extent of lateral shell compression. In a separate experiment, we found that snails raised in still water in a common garden showed higher resistance to water flow if originating from a wave environment than from a crab environment, and this was true both at juvenile (2 weeks) and adult (10 months) developmental stages. This result suggests genetic control of a distinct "wave adapted" phenotype, likely to be maintained under strong divergent selection between the two adjacent habitats.

What explains rare and conspicuous colours in a snail? A test of time-series data against models of drift, migration or selection.

Abstract: What explains rare and conspicuous colours in a snail? A test of time-series data against models of drift, migration or selection

Widespread hybridization within mound‐building wood ants in Southern Finland results in cytonuclear mismatches and potential for sex‐specific hybrid breakdown

Abstract: Hybridization and gene flow between diverging lineages is increasingly recognized as a common evolutionary process and its consequences can vary from hybrid breakdown to adaptive introgression. We have previously found a population of wood ant hybrids between Formica aquilonia and F. polyctena that shows antagonistic effects of hybridization: females with introgressed alleles show hybrid vigour, whereas males with the same alleles show hybrid breakdown. Here we investigate whether hybridization is a general phenomenon in this species pair, and analyze 647 worker samples from 16 localities in Finland using microsatellite markers and a 1200 bp mitochondrial sequence. Our results show that 27 sampled nests contained parental-like gene pools (six putative F. polyctena and 21 putative F. aquilonia) and all remaining nests (69), from nine localities, contained hybrids of varying degrees. Patterns of genetic variation suggest these hybrids arise from several hybridization events or, instead, have backcrossed to the parental gene pools to varying extents. In contrast to expectations, the mitochondrial haplotypes of the parental species were not randomly distributed among the hybrids. Instead, nests that were closer to parental-like F. aquilonia for nuclear markers preferentially had F. polyctena's mitochondria and vice versa. This systematic pattern suggests there may be underlying selection favoring cytonuclear mismatch and hybridization. We also found a new hybrid locality with strong genetic differences between the sexes similar to those predicted under antagonistic selection on male and female hybrids. Further studies are needed to determine the selective forces that act on male and female genomes in these newly discovered hybrids. This article is protected by copyright. All rights reserved.

Targeted re-sequencing confirms the importance of chemosensory genes in aphid host race differentiation

Abstract: Host-associated races of phytophagous insects provide a model for understanding how adaptation to a new environment can lead to reproductive isolation and speciation, ultimately enabling us to connect barriers to gene flow to adaptive causes of divergence. The pea aphid (Acyrthosiphon pisum) comprises host races specializing on legume species and provides a unique system for examining the early stages of diversification along a gradient of genetic and associated adaptive divergence. As host choice produces assortative mating, understanding the underlying mechanisms of choice will contribute directly to understanding of speciation. As host choice in the pea aphid is likely mediated by smell and taste, we use capture sequencing and SNP genotyping to test for the role of chemosensory genes in the divergence between eight host plant species across the continuum of differentiation and sampled at multiple locations across western Europe. We show high differentiation of chemosensory loci relative to control loci in a broad set of pea aphid races and localities, using a model-free approach based on principal component analysis. Olfactory and gustatory receptors form the majority of highly differentiated genes and include loci that were already identified as outliers in a previous study focusing on the three most closely related host races. Consistent indications that chemosensory genes may be good candidates for local adaptation and barriers to gene flow in the pea aphid open the way to further investigations aiming to understand their impact on gene flow and to determine their precise functions in response to host plant metabolites.

The chemical signatures underlying host plant discrimination by aphids

Abstract: The diversity of phytophagous insects is largely attributable to speciation involving shifts between host plants. These shifts are mediated by the close interaction between insects and plant metabolites. However, there has been limited progress in understanding the chemical signatures that underlie host preferences. We use the pea aphid (Acyrthosiphon pisum) to address this problem. Host-associated races of pea aphid discriminate between plant species in race-specific ways. We combined metabolomic profiling of multiple plant species with behavioural tests on two A. pisum races, to identify metabolites that explain variation in either acceptance or discrimination. Candidate compounds were identified using tandem mass spectrometry. Our results reveal a small number of compounds that explain a large proportion of variation in the differential acceptability of plants to A. pisum races. Two of these were identified as L-phenylalanine and L-tyrosine but it may be that metabolically-related compounds directly influence insect behaviour. The compounds implicated in differential acceptability were not related to the set correlated with general acceptability of plants to aphids, regardless of host race. Small changes in response to common metabolites may underlie host shifts. This study opens new opportunities for understanding the mechanistic basis of host discrimination and host shifts in insects.

Mechanisms of Adaptive Divergence and Speciation in Littorina saxatilis: Integrating Knowledge from Ecology and Genetics with New Data Emerging from Genomic Studies

Abstract: New opportunities to understand marine speciation and evolution of local adaptation come with genomic approaches and with the development of comprehensive model systems. The marine snail Littorina saxatilis is one example of a developing marine model for investigating genetic mechanisms of rapid divergence and evolution in natural systems. This species is strongly polymorphic and shows formation of local ecotypes throughout its distribution. Support is strong for primary (in situ) and parallel formation of reproductively semi-isolated ecotypes with contact zones between heterogeneous intertidal microhabitats. This makes this species an ideal organism for gaining new insights into the interplay of divergent selection, gene flow and genetic drift during local adaptation and speciation. A relatively well-resolved draft genome and a genetic map describing 17 linkage groups (“chromosomes”) are key tools for investigating the role of structural genomic variation, such as inversions, gene duplications and translocations. Whole genome re-sequencing of pools of individuals and the first comprehensive study of a contact zone contribute direct information on selection and barriers to gene flow present in specific regions of the genome. Linking selection at the phenotypic level to patterns obser ved in the genome is under way by quantitative trait loci mapping and annotation of candidate genes, while the role of single mutations on individual fitness will have to await development of gene manipulation tools. The features of the snail system facilitate the study of local adaptation and speciation and its genomic basis, but the underlying evolutionary processes are expected to be similar in other organisms, and hence this species is a useful model.

Genetic variation, selection and evolution: special issue in celebration of the 50th anniversary of the population genetics group meeting.

Abstract: Genetic variation, selection and evolution: special issue in celebration of the 50th anniversary of the population genetics group meeting

Inhibition of plasmin-mediated TAFI activation may affect development but not progression of abdominal aortic aneurysms.

Abstract: Objective: Thrombin-activatable fibrinolysis inhibitor (TAFI) reduces the breakdown of fibrin clots through its action as an indirect inhibitor of plasmin. Studies in TAFI-deficient mice have implicated a potential role for TAFI in Abdominal Aortic Aneurysm (AAA) disease. The role of TAFI inhibition on AAA formation in adult ApoE-/- mice is unknown. The aim of this paper was to investigate the effects of TAFI inhibition on AAA development and progression. Methods: Using the Angiotensin II model of AAA, male ApoE-/- mice were infused with Angiotensin II 750ng/kg/min with or without a monoclonal antibody inhibitor of plasmin-mediated activation of TAFI, MA-TCK26D6, or a competitive small molecule inhibitor of TAFI, UK-396082. Results: Inhibition of TAFI in the Angiotensin II model resulted in a decrease in the mortality associated with AAA rupture (from 40.0% to 16.6% with MA-TCK26D6 (log-rank Mantel Cox test p = 0.16), and 8.3% with UK-396082 (log-rank Mantel Cox test p = 0.05)). Inhibition of plasmin-mediated TAFI activation reduced the incidence of AAA from 52.4% to 30.0%. However, late treatment with MA-TCK26D6 once AAA were already established had no effect on the progression of AAA in this model. Conclusions: The formation of intra-mural thrombus is responsible for the dissection and early rupture in the angiotensin II model of AAA, and this process can be prevented through inhibition of TAFI. Late treatment with a TAFI inhibitor does not prevent AAA progression. These data may indicate a role for inhibition of plasmin-mediated TAFI activation in the early stages of AAA development, but not in its progression.

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

Abstract: In many diploid species the sex chromosomes play a special role in mediating reproductive isolation. In haplodiploids, where females are diploid and males haploid, the whole genome behaves similarly to the X/Z chromosomes of diploids. Therefore, haplodiploid systems can serve as a model for the role of sex chromosomes in speciation and hybridization. A previously described population of Finnish Formica wood ants displays genome-wide signs of ploidally and sexually antagonistic selection resulting from hybridization. Here, hybrid females have increased survivorship but hybrid males are inviable. To understand how the unusual hybrid population may be maintained, we developed a mathematical model with hybrid incompatibility, female heterozygote advantage, recombination, and assortative mating. The rugged fitness landscape resulting from the co-occurrence of heterozygote advantage and hybrid incompatibility results in a sexual conflict in haplodiploids, which is caused by the ploidy difference. Thus, whereas heterozygote advantage always promotes long-term polymorphism in diploids, we find various outcomes in haplodiploids in which the population stabilizes either in favor of males, females, or via maximizing the number of introgressed individuals. We discuss these outcomes with respect to the potential long-term fate of the Finnish wood ant population, and provide approximations for the extension of the model to multiple incompatibilities. Moreover, we highlight the general implications of our results for speciation and hybridization in haplodiploids versus diploids, and how the described fitness relationships could contribute to the outstanding role of sex chromosomes as hotspots of sexual antagonism and genes involved in speciation.