Lauren K. Lucas

GENOMIC REGIONS WITH A HISTORY OF DIVERGENT SELECTION AFFECT FITNESS OF HYBRIDS BETWEEN TWO BUTTERFLY SPECIES

Speciation is the process by which reproductively isolated lineages arise, and is one of the fundamental means by which the diversity of life increases. Whereas numerous studies have documented an association between ecological divergence and reproductive isolation, relatively little is known about the role of natural selection in genome divergence during the process of speciation. Here, we use genome‐wide DNA sequences and Bayesian models to test the hypothesis that loci under divergent selection between two butterfly species (Lycaeides idas and L. melissa) also affect fitness in an admixed population. Locus‐specific measures of genetic differentiation between L. idas and L. melissa and genomic introgression in hybrids varied across the genome. The most differentiated genetic regions were characterized by elevated L. idas ancestry in the admixed population, which occurs in L. idas‐like habitat, consistent with the hypothesis that local adaptation contributes to speciation. Moreover, locus‐specific measures of genetic differentiation (a metric of divergent selection) were positively associated with extreme genomic introgression (a metric of hybrid fitness). Interestingly, concordance of differentiation and introgression was only partial. We discuss multiple, complementary explanations for this partial concordance.

Secondary contact between Lycaeides idas and L. melissa in the Rocky Mountains: extensive admixture and a patchy hybrid zone.

Studies of hybridization have increased our understanding of the nature of species boundaries, the process of speciation, and the effects of hybridization on the evolution of populations and species. In the present study we use genetic and morphological data to determine the outcome and consequences of secondary contact and hybridization between the butterfly species Lycaeides idas and L. melissa in the Rocky Mountains. Admixture proportions estimated from structure and geographical cline analysis indicate L. idas and L. melissa have hybridized extensively in the Rocky Mountains and that reproductive isolation was insufficient to prevent introgression for much of the genome. Geographical patterns of admixture suggest that hybridization between L. idas and L. melissa has led to the formation of a hybrid zone. The hybrid zone is relatively wide, given estimates of dispersal for Lycaeides butterflies, and does not show strong evidence of cline concordance among characters. We believe the structure of the Lycaeides hybrid zone might be best explained by the patchy distribution of Lycaeides, local extinction and colonization of habitat patches, environmental variation and weak overall selection against hybrids. We found no evidence that hybridization in the Rocky Mountains has resulted in the formation of independent hybrid species, in contrast to the outcome of hybridization between L. idas and L. melissa in the Sierra Nevada. Finally, our results suggest that differences in male morphology between L. idas and L. melissa might contribute to isolation, or perhaps even that selection has favoured the spread of L. melissa male genitalia alleles.

Admixture and the organization of genetic diversity in a butterfly species complex revealed through common and rare genetic variants

Detailed information about the geographic distribution of genetic and genomic variation is necessary to better understand the organization and structure of biological diversity. In particular, spatial isolation within species and hybridization between them can blur species boundaries and create evolutionary relationships that are inconsistent with a strictly bifurcating tree model. Here, we analyse genome‐wide DNA sequence and genetic ancestry variation in Lycaeides butterflies to quantify the effects of admixture and spatial isolation on how biological diversity is organized in this group. We document geographically widespread and pervasive historical admixture, with more restricted recent hybridization. This includes evidence supporting previously known and unknown instances of admixture. The genome composition of admixed individuals varies much more among than within populations, and tree‐ and genetic ancestry‐based analyses indicate that multiple distinct admixed lineages or populations exist. We find that most genetic variants in Lycaeides are rare (minor allele frequency <0.5%). Because the spatial and taxonomic distributions of alleles reflect demographic and selective processes since mutation, rare alleles, which are presumably younger than common alleles, were spatially and taxonomically restricted compared with common variants. Thus, we show patterns of genetic variation in this group are multifaceted, and we argue that this complexity challenges simplistic notions concerning the organization of biological diversity into discrete, easily delineated and hierarchically structured entities.

The evolution of novel host use is unlikely to be constrained by trade‐offs or a lack of genetic variation

The genetic and ecological factors that shape the evolution of animal diets remain poorly understood. For herbivorous insects, the expectation has been that trade‐offs exist, such that adaptation to one host plant reduces performance on other potential hosts. We investigated the genetic architecture of alternative host use by rearing individual Lycaeides melissa butterflies from two wild populations in a crossed design on two hosts (one native and one introduced) and analysing the genetic basis of differences in performance using genomic approaches. Survival during the experiment was highest when butterfly larvae were reared on their natal host plant, consistent with local adaptation. However, cross‐host correlations in performance among families (within populations) were not different from zero. We found that L. melissa populations possess genetic variation for larval performance and variation in performance had a polygenic basis. We documented very few genetic variants with trade‐offs that would inherently constrain diet breadth by preventing the optimization of performance across hosts. Instead, most genetic variants that affected performance on one host had little to no effect on the other host. In total, these results suggest that genetic trade‐offs are not the primary cause of dietary specialization in L. melissa butterflies.

HYBRID SPECIATION AND INDEPENDENT EVOLUTION IN LINEAGES OF ALPINE BUTTERFLIES

The power of hybridization between species to generate variation and fuel adaptation is poorly understood despite long‐standing interest. There is, however, increasing evidence that hybridization often generates biodiversity, including via hybrid speciation. We tested the hypothesis of hybrid speciation in butterflies occupying extreme, high‐altitude habitats in four mountain ranges in western North America with an explicit, probabilistic model, and genome‐wide DNA sequence data. Using this approach, in concert with ecological experiments and observations and morphological data, we document three lineages of hybrid origin. These lineages have different genome admixture proportions and distinctive trait combinations that suggest unique and independent evolutionary histories.

GENOME DIVERGENCE AND THE GENETIC ARCHITECTURE OF BARRIERS TO GENE FLOW BETWEEN LYCAEIDES IDAS AND L. MELISSA

Genome divergence during speciation is a dynamic process that is affected by various factors, including the genetic architecture of barriers to gene flow. Herein we quantitatively describe aspects of the genetic architecture of two sets of traits, male genitalic morphology and oviposition preference, that putatively function as barriers to gene flow between the butterfly species Lycaeides idas and L. melissa. Our analyses are based on unmapped DNA sequence data and a recently developed Bayesian regression approach that includes variable selection and explicit parameters for the genetic architecture of traits. A modest number of nucleotide polymorphisms explained a small to large proportion of the variation in each trait, and average genetic variant effects were nonnegligible. Several genetic regions were associated with variation in multiple traits or with trait variation within‐ and among‐populations. In some instances, genetic regions associated with trait variation also exhibited exceptional genetic differentiation between species or exceptional introgression in hybrids. These results are consistent with the hypothesis that divergent selection on male genitalia has contributed to heterogeneous genetic differentiation, and that both sets of traits affect fitness in hybrids. Although these results are encouraging, we highlight several difficulties related to understanding the genetics of speciation.

Patterns of Genitalic Morphology Around Suture Zones in North American Lycaeides (Lepidoptera: Lycaenidae): Implications for Taxonomy and Historical Biogeography

Abstract Within the North American Lycaeides (Hübner) fauna, there are at least three major lineages that exhibit extensive morphological and ecological variation, especially at suture zones where these lineages meet. We examined male genitalic morphology in Lycaeides populations spanning much of North America to evaluate the current taxonomy and to address questions about the patterns of morphological variation at suture zones and potential evolutionary processes responsible for the patterns. Our genitalic measurements were based on those of V. Nabokov who revised North American Lycaeides taxonomy in the 1940s. Canonical discriminant analysis validated Nabokov’s original species designations, but it did not support many of his subspecific designations. Populations at a suture zone in the Great Lakes region are similar to populations on the east side of this zone. Populations at a western suture zone in the Sierra Nevada and adjacent ranges exhibit intermediate morphology between lineages on either side of this suture zone. We tested the hypothesis that contemporary gene flow contributes to the patterns of morphology in suture zones by testing for the increased variance in quantitative traits that is expected in a hybrid swarm. Based on a comparison of variances from populations within and outside of these suture zones, there is no evidence of current hybridization between lineages, with the sole exception of the population sample from the White Mountains of eastern California. The intermediate morphology and the general absence of increased variance within western suture zone populations imply that hybridization may have been important in the evolution of North American Lycaeides.

Geographic and genetic isolation in spring-associated Eurycea salamanders endemic to the Edwards Plateau region of Texas

Populations of neotenic, spring-associated salamanders of the genus Eurycea occupy discontinuous sites throughout the Edwards Plateau of central Texas and many warrant conservation attention. Here we used DNA sequence data from a nuclear (rag1) and a mitochondrial (ND4) gene to determine (1) the extent of genetic isolation among seven Edwards Plateau Eurycea populations and (2) the relationship between genetic distance and both geographic distance and hydrogeological features. Coalescent-based methods detected little gene flow among the sampled Eurycea populations, and we were unable to reject a model of complete isolation for any pair of populations. These findings were consistent with the relatively high genetic distances we detected among the sampled Eurycea populations (pairwise ϕST ranged from 0.249 to 0.924). We detected a positive correlation between genetic distance and geographic distance, which is consistent with a pattern of isolation by distance. However, while controlling for geographic distance, we did not detect a positive relationship between genetic distance and aquifer or river distance. Thus, we found no evidence that aquifers and/or rivers serve as dispersal corridors among isolated Eurycea populations. Based on these results, we have no evidence that re-colonization of spring sites by migrant salamanders following local extirpation would be likely. Our findings indicate that spring-associated Eurycea salamander populations occupying the Edwards Plateau region are genetically isolated, and that each of these populations should be considered a distinct management unit.

Geographically multifarious phenotypic divergence during speciation

Speciation is an important evolutionary process that occurs when barriers to gene flow evolve between previously panmictic populations. Although individual barriers to gene flow have been studied extensively, we know relatively little regarding the number of barriers that isolate species or whether these barriers are polymorphic within species. Herein, we use a series of field and lab experiments to quantify phenotypic divergence and identify possible barriers to gene flow between the butterfly species Lycaeides idas and Lycaeides melissa. We found evidence that L. idas and L. melissa have diverged along multiple phenotypic axes. Specifically, we identified major phenotypic differences in female oviposition preference and diapause initiation, and more moderate divergence in mate preference. Multiple phenotypic differences might operate as barriers to gene flow, as shown by correlations between genetic distance and phenotypic divergence and patterns of phenotypic variation in admixed Lycaeides populations. Although some of these traits differed primarily between species (e.g., diapause initiation), several traits also varied among conspecific populations (e.g., male mate preference and oviposition preference).

Genetic architecture, biochemical underpinnings and ecological impact of floral UV patterning

Floral attraction traits can significantly affect pollinator visitation patterns, but adaptive evolution of these traits may be constrained by correlations with other traits. In some cases, molecular pathways contributing to floral attraction are well characterized, offering the opportunity to explore loci potentially underlying variation among individuals. Here, we quantify the range of variation in floral UV patterning (i.e. UV ‘bulls‐eye nectar guides) among crop and wild accessions of Brassica rapa. We then use experimental crosses to examine the genetic architecture, candidate loci and biochemical underpinnings of this patterning as well as phenotypic manipulations to test the ecological impact. We find qualitative variation in UV patterning between wild (commonly lacking UV patterns) and crop (commonly exhibiting UV patterns) accessions. Similar to the majority of crops, recombinant inbred lines (RILs) derived from an oilseed crop × WI fast‐plant® cross exhibit UV patterns, the size of which varies extensively among genotypes. In RILs, we further observe strong statistical‐genetic and QTL correlations within petal morphological traits and within measurements of petal UV patterning; however, correlations between morphology and UV patterning are weak or nonsignificant, suggesting that UV patterning is regulated and may evolve independently of overall petal size. HPLC analyses reveal a high concentration of sinapoyl glucose in UV‐absorbing petal regions, which, in concert with physical locations of UV‐trait QTLs, suggest a regulatory and structural gene as candidates underlying observed quantitative variation. Finally, insects prefer flowers with UV bulls‐eye patterns over those that lack patterns, validating the importance of UV patterning in pollen‐limited populations of B. rapa.