The relative impact of evolving pleiotropy and mutational correlation on trait divergence

Both pleiotropic connectivity and mutational correlations can restrict the decoupling of traits under divergent selection, but it is unknown which is more important in trait evolution. To address this question, we create a model that permits within-population variation in both pleiotropic connectivity and mutational correlation, and compare their relative importance to trait evolution. Specifically, we developed an individual-based stochastic model where mutations can affect whether a locus affects a trait and the extent of mutational correlations in a population. We find that traits can decouple whether there is evolution in pleiotropic connectivity or mutational correlation, but when both can evolve, then evolution in pleiotropic connectivity is more likely to allow for decoupling to occur. The most common genotype found in this case is characterized by having one locus that maintains connectivity to all traits and another that loses connectivity to the traits under stabilizing selection (subfunctionalization). This genotype is favored because it allows the subfunctionalized locus to accumulate greater effect size alleles, contributing to increasingly divergent trait values in the traits under divergent selection without changing the trait values of the other traits (genetic modularization). These results provide evidence that partial subfunctionalization of pleiotropic loci may be a common mechanism of trait decoupling under regimes of corridor selection.

Neurogenomic divergence during speciation by reinforcement of mating behaviors in chorus frogs (Pseudacris)

Background Species interactions can promote mating behavior divergence, particularly when these interactions are costly due to maladaptive hybridization. Selection against hybridization can indirectly cause evolution of reproductive isolation within species, a process termed cascade reinforcement. This process can drive incipient speciation by generating divergent selection pressures among populations that interact with different species assemblages. Theoretical and empirical studies indicate that divergent selection on gene expression networks has the potential to increase reproductive isolation among populations. After identifying candidate synaptic transmission genes derived from neurophysiological studies in anurans, we test for divergence of gene expression in a system undergoing cascade reinforcement, the Upland Chorus Frog (Pseudacris feriarum). Results Our analyses identified seven candidate synaptic transmission genes that have diverged between ancestral and reinforced populations of P. feriarum, including five that encode synaptic vesicle proteins. Our gene correlation network analyses revealed four genetic modules that have diverged between these populations, two possessing a significant concentration of neurotransmission enrichment terms: one for synaptic membrane components and the other for metabolism of the neurotransmitter nitric oxide. We also ascertained that a greater number of genes have diverged in expression by geography than by sex. Moreover, we found that more genes have diverged within females as compared to males between populations. Conversely, we observed no difference in the number of differentially-expressed genes within the ancestral compared to the reinforced population between the sexes. Conclusions This work is consistent with the idea that divergent selection on mating behaviors via cascade reinforcement contributed to evolution of gene expression in P. feriarum. Although our study design does not allow us to fully rule out the influence of environment and demography, the fact that more genes diverged in females than males points to a role for cascade reinforcement. Our discoveries of divergent candidate genes and gene networks related to neurotransmission support the idea that neural mechanisms of acoustic mating behaviors have diverged between populations, and agree with previous neurophysiological studies in frogs. Increasing support for this hypothesis, however, will require additional experiments under common garden conditions. Our work points to the importance of future replicated and tissue-specific studies to elucidate the relative contribution of gene expression divergence to the evolution of reproductive isolation during incipient speciation.

Connecting the past, present and future: A population genomic study of Australasian snapper (Chrysophrys auratus) in New Zealand

<p><b>Advances in genomic methods now enable the study of wild populations and their evolutionary history at an unprecedented level. The genotyping of many thousands of genetic markers across the genome provides high statistical resolution. This enables the identification of adaptive genetic variation, providing novel insights into population demography and the processes driving population divergence. Marine fish are ideal candidates to study the processes driving evolutionary divergence because selection works efficiently in large populations, and marine populations can be distributed over large spatial ranges and occupy a range of environmental conditions. This thesis used whole-genome variant data to study the Australasian snapper (Chrysophrys auratus, tāmure) in New Zealand. Snapper is one of New Zealand’s largest inshore fisheries and has experienced significant population reductions. The aims of this thesis were to investigate the genome-wide variation in snapper in New Zealand and 1) assess the neutral and adaptive population genetic structure, 2) reconstruct the demographic history, and 3) identify genomic regions, genes and their functions that show signs of selection.</b></p> <p>Population genomic structure was assessed using whole-genome resequencing data from 350 individuals, and this data set resulted in 167,543 assumed neutrally evolving loci (SNPs). It was found that levels of genetic diversity were not significantly different between populations, suggesting that fishing pressure has not lead to local reductions in genetic variation. Levels of genetic differentiation between sampled populations was low, with significant evidence for isolation by distance (R2 = 0.75, p = 0.002). Pairwise FST estimates and PCA/DAPC showed the presence of two genetic clusters, one containing the northern and one containing the southern populations. Genetic disjunctions combined with mixing between the clusters was detected around the Mahia peninsula and Cape Reinga. The identification of adaptive loci enabled the identification of fine-scale population structure, reflecting currently recognized stocks. The ability to differentiate between stocks is fundamental for fisheries management. The patterns detected here show promising results for future implementation into fisheries management of snapper stocks.</p> <p>Contemporary and ancient mitochondrial genomes were used to assess the demographic, and phylogeographic history of snapper. Analyses indicated that haplotype diversity was high (0.968-0.982), which is commonly observed in species with large populations sizes. Mitochondrial genomes showed the presence of two lineages that diverged approximately 650,000 (490,000 – 840,000) years ago. The separation was likely linked to reductions in sea level during glacial cycles. Estimates of changes in population size show strong support for an exponential population size increase after the last glacial maximum (LGM). Changes in population abundance based on the Bayesian Skyline plot indicated a strong population increase approximately 10,000 years ago. The steep increase in new branches in the phylogenetic tree suggests population sizes increase approximately 20,000 (7,000-35,000) years ago. A post-glacial expansion is the most likely explanation for the observed increase in population abundance. During this period, sea levels rose which presumably reconnected fragmented populations, and subsequent increased sea temperatures allowed for southward expansion.</p> <p>Whole-genome sequences from contemporary snapper populations were used to identify genes under selection. Analyses were conducted to detect selection in a single genetic cluster (divergent selection), or both genetic clusters (nation-wide selection). In total, 101 genomic regions containing 253 different genes showed evidence for selection. Two genomic regions showed strong evidence for divergent selection between the northern and southern cluster (FST > 0.2). The regions contained two genes associated with glycolysis which are linked to (cell-) growth (i.e. mast2 and hk2). The regions containing hk2 showed a lack of rare alleles (TD > 2) in the southern cluster, consistent with balancing selection maintaining multiple alleles in the population. Variation in growth rate may be maintained throughout the genetic cluster because of a latitudinal gradient in sea temperature. Strong evidence for selective sweeps were detected in two genomic regions on a nation-wide level. Both regions contained genes associated with angiogenesis (mydgf and rnf213a), which has been shown to affect maturation in species of fish. While tentative, it is possible that intense size-selective fishing is selecting for early maturation in snapper, a life life-history commonly associated with fishing-induced evolution. A selection scan contrasting the population Tasman Bay and Karamea Bight was performed to test for evidence of adaption to cold stress. Selection was detected in 123 genomic regions containing 296 genes, of which 197 potentially experience divergent selection. Two genes were located in regions that showed significant evidence of selection (camk2g and ksr2). Both genes have been associated with cold stress in previous studies, suggesting the Karamea Bight could represent an adaptive front at the southern range of the distribution of snapper.</p> <p>This thesis presents the first population genomic study of Australasian snapper in New Zealand, a species with a diverse genetic landscape and a rich evolutionary history. The detection of fine-scale population structure through adaptive differences between populations highlights the promising application of genomics in fisheries management. The study of mitochondrial lineages showed the effect of glacial cycles, providing insights into how New Zealand’s marine fauna has been affected by major changes in global climate. Finally, the identification of genes and associated biological traits under selection has provided fundamental new insights regarding the environmental conditions that drive adaptive change and act on phenotypes. Snapper is an ideal species for developing and integrating genomics into New Zealand fisheries management. A detailed understanding of fish stock demography and adaptive potential is critical to support improvement to fisheries management as wild stocks continue to face strong anthropogenic pressures (e.g. climate change and overexploitation). Genomics provides valuable insights into how stock assessments and harvesting levels can be better set to match the natural biological units of a species that are determined by gene flow and adaptive variation.</p>

Connecting the past, present and future: A population genomic study of Australasian snapper (Chrysophrys auratus) in New Zealand

<p><b>Advances in genomic methods now enable the study of wild populations and their evolutionary history at an unprecedented level. The genotyping of many thousands of genetic markers across the genome provides high statistical resolution. This enables the identification of adaptive genetic variation, providing novel insights into population demography and the processes driving population divergence. Marine fish are ideal candidates to study the processes driving evolutionary divergence because selection works efficiently in large populations, and marine populations can be distributed over large spatial ranges and occupy a range of environmental conditions. This thesis used whole-genome variant data to study the Australasian snapper (Chrysophrys auratus, tāmure) in New Zealand. Snapper is one of New Zealand’s largest inshore fisheries and has experienced significant population reductions. The aims of this thesis were to investigate the genome-wide variation in snapper in New Zealand and 1) assess the neutral and adaptive population genetic structure, 2) reconstruct the demographic history, and 3) identify genomic regions, genes and their functions that show signs of selection.</b></p> <p>Population genomic structure was assessed using whole-genome resequencing data from 350 individuals, and this data set resulted in 167,543 assumed neutrally evolving loci (SNPs). It was found that levels of genetic diversity were not significantly different between populations, suggesting that fishing pressure has not lead to local reductions in genetic variation. Levels of genetic differentiation between sampled populations was low, with significant evidence for isolation by distance (R2 = 0.75, p = 0.002). Pairwise FST estimates and PCA/DAPC showed the presence of two genetic clusters, one containing the northern and one containing the southern populations. Genetic disjunctions combined with mixing between the clusters was detected around the Mahia peninsula and Cape Reinga. The identification of adaptive loci enabled the identification of fine-scale population structure, reflecting currently recognized stocks. The ability to differentiate between stocks is fundamental for fisheries management. The patterns detected here show promising results for future implementation into fisheries management of snapper stocks.</p> <p>Contemporary and ancient mitochondrial genomes were used to assess the demographic, and phylogeographic history of snapper. Analyses indicated that haplotype diversity was high (0.968-0.982), which is commonly observed in species with large populations sizes. Mitochondrial genomes showed the presence of two lineages that diverged approximately 650,000 (490,000 – 840,000) years ago. The separation was likely linked to reductions in sea level during glacial cycles. Estimates of changes in population size show strong support for an exponential population size increase after the last glacial maximum (LGM). Changes in population abundance based on the Bayesian Skyline plot indicated a strong population increase approximately 10,000 years ago. The steep increase in new branches in the phylogenetic tree suggests population sizes increase approximately 20,000 (7,000-35,000) years ago. A post-glacial expansion is the most likely explanation for the observed increase in population abundance. During this period, sea levels rose which presumably reconnected fragmented populations, and subsequent increased sea temperatures allowed for southward expansion.</p> <p>Whole-genome sequences from contemporary snapper populations were used to identify genes under selection. Analyses were conducted to detect selection in a single genetic cluster (divergent selection), or both genetic clusters (nation-wide selection). In total, 101 genomic regions containing 253 different genes showed evidence for selection. Two genomic regions showed strong evidence for divergent selection between the northern and southern cluster (FST > 0.2). The regions contained two genes associated with glycolysis which are linked to (cell-) growth (i.e. mast2 and hk2). The regions containing hk2 showed a lack of rare alleles (TD > 2) in the southern cluster, consistent with balancing selection maintaining multiple alleles in the population. Variation in growth rate may be maintained throughout the genetic cluster because of a latitudinal gradient in sea temperature. Strong evidence for selective sweeps were detected in two genomic regions on a nation-wide level. Both regions contained genes associated with angiogenesis (mydgf and rnf213a), which has been shown to affect maturation in species of fish. While tentative, it is possible that intense size-selective fishing is selecting for early maturation in snapper, a life life-history commonly associated with fishing-induced evolution. A selection scan contrasting the population Tasman Bay and Karamea Bight was performed to test for evidence of adaption to cold stress. Selection was detected in 123 genomic regions containing 296 genes, of which 197 potentially experience divergent selection. Two genes were located in regions that showed significant evidence of selection (camk2g and ksr2). Both genes have been associated with cold stress in previous studies, suggesting the Karamea Bight could represent an adaptive front at the southern range of the distribution of snapper.</p> <p>This thesis presents the first population genomic study of Australasian snapper in New Zealand, a species with a diverse genetic landscape and a rich evolutionary history. The detection of fine-scale population structure through adaptive differences between populations highlights the promising application of genomics in fisheries management. The study of mitochondrial lineages showed the effect of glacial cycles, providing insights into how New Zealand’s marine fauna has been affected by major changes in global climate. Finally, the identification of genes and associated biological traits under selection has provided fundamental new insights regarding the environmental conditions that drive adaptive change and act on phenotypes. Snapper is an ideal species for developing and integrating genomics into New Zealand fisheries management. A detailed understanding of fish stock demography and adaptive potential is critical to support improvement to fisheries management as wild stocks continue to face strong anthropogenic pressures (e.g. climate change and overexploitation). Genomics provides valuable insights into how stock assessments and harvesting levels can be better set to match the natural biological units of a species that are determined by gene flow and adaptive variation.</p>

Ancestral polymorphisms shape the adaptive radiation of Metrosideros across the Hawaiian Islands

Some of the most spectacular adaptive radiations begin with founder populations on remote islands. How genetically limited founder populations give rise to the striking phenotypic and ecological diversity characteristic of adaptive radiations is a paradox of evolutionary biology. We conducted an evolutionary genomics analysis of genus Metrosideros, a landscape-dominant, incipient adaptive radiation of woody plants that spans a striking range of phenotypes and environments across the Hawaiian Islands. Using nanopore-sequencing, we created a chromosome-level genome assembly for Metrosideros polymorpha var. incana and analyzed whole-genome sequences of 131 individuals from 11 taxa sampled across the islands. Demographic modeling and population genomics analyses suggested that Hawaiian Metrosideros originated from a single colonization event and subsequently spread across the archipelago following the formation of new islands. The evolutionary history of Hawaiian Metrosideros shows evidence of extensive reticulation associated with significant sharing of ancestral variation between taxa and secondarily with admixture. Taking advantage of the highly contiguous genome assembly, we investigated the genomic architecture underlying the adaptive radiation and discovered that divergent selection drove the formation of differentiation outliers in paired taxa representing early stages of speciation/divergence. Analysis of the evolutionary origins of the outlier single nucleotide polymorphisms (SNPs) showed enrichment for ancestral variations under divergent selection. Our findings suggest that Hawaiian Metrosideros possesses an unexpectedly rich pool of ancestral genetic variation, and the reassortment of these variations has fueled the island adaptive radiation.

Genomic signatures of spatially divergent selection at clownfish range margins

Understanding how evolutionary forces interact to drive patterns of selection and distribute genetic variation across a species' range is of great interest in ecology and evolution, especially in an era of global change. While theory predicts how and when populations at range margins are likely to undergo local adaptation, empirical evidence testing these models remains sparse. Here, we address this knowledge gap by investigating the relationship between selection, gene flow and genetic drift in the yellowtail clownfish, Amphiprion clarkii, from the core to the northern periphery of the species range. Analyses reveal low genetic diversity at the range edge, gene flow from the core to the edge and genomic signatures of local adaptation at 56 single nucleotide polymorphisms in 25 candidate genes, most of which are significantly correlated with minimum annual sea surface temperature. Several of these candidate genes play a role in functions that are upregulated during cold stress, including protein turnover, metabolism and translation. Our results illustrate how spatially divergent selection spanning the range core to the periphery can occur despite the potential for strong genetic drift at the range edge and moderate gene flow from the core populations.