Rapid evolution of novel biotic interactions in the UK Brown Argus butterfly uses genomic variation from across its geographical range.

Understanding the rate and extent to which populations can adapt to novel environments at their ecological margins is fundamental to predicting the persistence of biological communities during ongoing and rapid global change. Recent range expansion in response to climate change in the UK butterfly Aricia agestis is associated with the evolution of novel interactions with a larval food plant, and the loss of its ability to use an ancestral host species. Using ddRAD analysis of 61,210 variable SNPs from 261 females from throughout the UK range of this species, we identify genomic regions at multiple chromosomes that are associated with evolutionary responses, and their association with demographic history and ecological variation. Gene flow appears widespread throughout the range, despite the apparently fragmented nature of the habitats used by this species. Patterns of haplotype variation between selected and neutral genomic regions suggest that evolution associated with climate adaptation is polygenic, resulting from the independent spread of alleles throughout the established range of this species, rather than the colonization of pre-adapted genotypes from coastal populations. These data suggest that rapid responses to climate change do not depend on the availability of pre-adapted genotypes. Instead, the evolution of novel forms of biotic interaction in A. agestis has occurred during range expansion, through the assembly of novel genotypes from alleles from multiple localities.

Recovering individual haplotypes and a contiguous genome assembly from pooled long-read sequencing of the diamondback moth (Lepidoptera: Plutellidae).

The assembly of divergent haplotypes using noisy long-read data presents a challenge to the reconstruction of haploid genome assemblies, due to overlapping distributions of technical sequencing error, intralocus genetic variation, and interlocus similarity within these data. Here, we present a comparative analysis of assembly algorithms representing overlap-layout-consensus, repeat graph, and de Bruijn graph methods. We examine how postprocessing strategies attempting to reduce redundant heterozygosity interact with the choice of initial assembly algorithm and ultimately produce a series of chromosome-level assemblies for an agricultural pest, the diamondback moth, Plutella xylostella (L.). We compare evaluation methods and show that BUSCO analyses may overestimate haplotig removal processing in long-read draft genomes, in comparison to a k-mer method. We discuss the trade-offs inherent in assembly algorithm and curation choices and suggest that "best practice" is research question dependent. We demonstrate a link between allelic divergence and allele-derived contig redundancy in final genome assemblies and document the patterns of coding and noncoding diversity between redundant sequences. We also document a link between an excess of nonsynonymous polymorphism and haplotigs that are unresolved by assembly or postassembly algorithms. Finally, we discuss how this phenomenon may have relevance for the usage of noisy long-read genome assemblies in comparative genomics.

Recessive Z-linked lethals and the retention of haplotype diversity in a captive butterfly population.

Sex chromosomes are predicted to harbour elevated levels of sexually antagonistic variation due to asymmetries in the heritability of recessive traits in the homogametic versus heterogametic sex. This evolutionary dynamic may manifest as high recessive load specifically affecting the homogametic sex, and the retention of haplotype diversity in small populations. We tested the hypothesis that the Z chromosome in the butterfly Bicyclus anynana carries a high inbred load for male fertility and viability. Homozygosity of Z chromosome blocks was produced by daughter-father backcrosses, and inferred from marker loci positioned via a linkage map. Male sterility was, in general, unrelated to homozygosity in any region of the Z, but there was an extreme deficit of homozygous males within a 2 cM interval in all families. In contrast, no corresponding skew in Z genotype was detected in their (hemizygous) sisters. The same pattern was observed in historically inbred lines, indicating a high frequency of recessive lethals in the ancestral population. Allele-frequency changes between 1993 and 2006 (70 generations at Ne ~ 160) show that, despite the loss of many haplotypes, diversity was retained significantly above the neutral expectation. Effective overdominance in the lethal region can account for this effect locally but not in other parts of the chromosome, that are also associated with persistent linkage disequilibrium. These unexpected patterns suggest the operation of other factors, such as epistatic selection, recombination suppression, assortative mating and meiotic drive. Our results highlight the role of balancing selection in maintaining the inbred load and linked genetic diversity.