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Kronforst, Marcus; Connallon, Tim (Ed.)Abstract Investigations into the genetic basis of color polymorphism have played a key role in our understanding of genetic architecture and the evolution of mating systems. Sulfur butterflies (Colias) have been models in this field, but also contain unsolved puzzles with respect to species boundaries and hybridization. We surveyed genomic variation across 5 years in a location where phenotypic intermediates between Colias eurytheme and C. eriphyle are observed, but ancestry variation of potential hybrids has not been quantified. Our results reveal individuals with hybrid ancestry roughly in proportion to the frequency of individuals of intermediate phenotype recorded in the wild. Individuals with hybrid ancestry were predominantly those with intermediate morphologies, but morphologically intermediate individuals were not always of hybrid origin, which raises alternative possibilities for the origin and maintenance of color variation in the system. Genomic regions differentiated between species are largely located on the Z chromosome, and we find more candidates on autosomes than in another Colias contact zone. The dynamics of hybridization in this system are highly variable through time, suggesting fertile avenues for future study into the maintenance of species boundaries in the face of temporally variable, climatically influenced, and pervasive hybridization.more » « lessFree, publicly-accessible full text available April 14, 2027
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Structural elements are widespread across genomes, but their complexity and role in repeatedly driving local adaptation remain unclear. In this work, we use phased genome assemblies to show that adaptive divergence in cryptic color pattern in a stick insect is repeatedly underlain by structural variation, but not a simple chromosomal inversion. We found that color pattern in populations of stick insects on two mountains is associated with translocations that have also been inverted. These translocations differ in size and origin on each mountain, but they overlap partially and involve some of the same gene regions. Moreover, this structural variation is subject to divergent selection and arose without introgression between species. Our results show how the origin of structural variation provides a mechanism for repeated bouts of adaptation.more » « less
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The extent to which evolution is repeatable remains debated. Here, we study changes over time in the frequency of cryptic color-pattern morphs in 10 replicate long-term field studies of a stick insect, each spanning at least a decade (across 30 years of total data). We find predictable “up-and-down” fluctuations in stripe frequency in all populations, representing repeatable evolutionary dynamics based on standing genetic variation. A field experiment demonstrates that these fluctuations involve negative frequency-dependent natural selection (NFDS). These fluctuations rely on demographic and selective variability that pushes populations away from equilibrium, such that they can reliably move back toward it via NFDS. Last, we show that the origin of new cryptic forms is associated with multiple structural genomic variants such that which mutations arise affects evolution at larger temporal scales. Thus, evolution from existing variation is predictable and repeatable, but mutation adds complexity even for traits evolving deterministically under natural selection.more » « less
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Abstract Hybridization is a common process that has broadly impacted the evolution of multicellular eukaryotes; however, how ecological factors influence this process remains poorly understood. Here, we report the findings of a 3-year recapture study of the Bryant’s woodrat (Neotoma bryanti) and desert woodrat (Neotoma lepida), two species that hybridize within a creosote bush (Larrea tridentata) shrubland in Whitewater, CA, USA. We used a genotype-by-sequencing approach to characterize the ancestry distribution of individuals across this hybrid zone coupled with Cormack–Jolly–Seber modeling to describe demography. We identified a high frequency of hybridization at this site with ~40% of individuals possessing admixed ancestry, which is the result of multigenerational backcrossing and advanced hybrid-hybrid crossing. F1, F2, and advanced generation hybrids had apparent survival rates similar to parental N. bryanti, while parental and backcross N. lepida had lower apparent survival rates and were far less abundant. Compared to bimodal hybrid zones where hybrids are often rare and selected against, we find that hybrids at Whitewater are common and have comparable survival to the dominant parental species, N. bryanti. The frequency of hybridization at Whitewater is therefore likely limited by the abundance of the less common parental species, N. lepida, rather than selection against hybrids.more » « less
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Identifying the genetic basis of adaptation is a central goal of evolutionary biology. However, identifying genes and mutations affecting fitness remains challenging because a large number of traits and variants can influence fitness. Selected phenotypes can also be difficult to know a priori , complicating top–down genetic approaches for trait mapping that involve crosses or genome-wide association studies. In such cases, experimental genetic approaches, where one maps fitness directly and attempts to infer the traits involved afterwards, can be valuable. Here, we re-analyse data from a transplant experiment involving Timema stick insects, where five physically clustered single-nucleotide polymorphisms associated with cryptic body coloration were shown to interact to affect survival. Our analysis covers a larger genomic region than past work and revealed a locus previously not identified as associated with survival. This locus resides near a gene, Punch ( Pu ) , involved in pteridine pigments production, implying that it could be associated with an unmeasured coloration trait. However, by combining previous and newly obtained phenotypic data, we show that this trait is not eye or body coloration. We discuss the implications of our results for the discovery of traits, genes and mutations associated with fitness in other systems, as well as for supergene evolution. This article is part of the theme issue ‘Genetic basis of adaptation and speciation: from loci to causative mutations’.more » « less
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Abstract Background Distributional responses by alpine taxa to repeated, glacial-interglacial cycles throughout the last two million years have significantly influenced the spatial genetic structure of populations. These effects have been exacerbated for the American pika ( Ochotona princeps ), a small alpine lagomorph constrained by thermal sensitivity and a limited dispersal capacity. As a species of conservation concern, long-term lack of gene flow has important consequences for landscape genetic structure and levels of diversity within populations. Here, we use reduced representation sequencing (ddRADseq) to provide a genome-wide perspective on patterns of genetic variation across pika populations representing distinct subspecies. To investigate how landscape and environmental features shape genetic variation, we collected genetic samples from distinct geographic regions as well as across finer spatial scales in two geographically proximate mountain ranges of eastern Nevada. Results Our genome-wide analyses corroborate range-wide, mitochondrial subspecific designations and reveal pronounced fine-scale population structure between the Ruby Mountains and East Humboldt Range of eastern Nevada. Populations in Nevada were characterized by low genetic diversity (π = 0.0006–0.0009; θ W = 0.0005–0.0007) relative to populations in California (π = 0.0014–0.0019; θ W = 0.0011–0.0017) and the Rocky Mountains (π = 0.0025–0.0027; θ W = 0.0021–0.0024), indicating substantial genetic drift in these isolated populations. Tajima’s D was positive for all sites ( D = 0.240–0.811), consistent with recent contraction in population sizes range-wide. Conclusions Substantial influences of geography, elevation and climate variables on genetic differentiation were also detected and may interact with the regional effects of anthropogenic climate change to force the loss of unique genetic lineages through continued population extirpations in the Great Basin and Sierra Nevada.more » « less
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