Rates and patterns of genome evolution in Lepidoptera

Abstract: The evolutionary consequences of genome restructuring and chromosomal rearrangements can be significant, but the underlying mechanisms are poorly understood. This thesis explores the relationships between genome restructuring, recombination, and maintenance of genetic diversity in different butterfly species. I also investigate the genetic underpinnings of different types of adaptations in two butterfly species with distinct life-history characteristics and adaptations. In Chapter I, whole genome alignments and linkage maps were used to characterize inter- and intra-specific chromosomal rearrangements in wood white butterflies (Leptidea spp.), revealing extensive reorganization of the chromosomes predominantly driven by fusions and fissions. Several fusion-fission polymorphisms were found segregating within populations, confirming the dynamic and ongoing process of karyotype evolution. In Chapter II, I used the linkage map information to show that chromosomal rearrangements have had considerable effects on the recombination landscape and maintenance of genetic diversity. Chapter III presents a detailed annotation of the genome of a long-distance migrant, the painted lady butterfly (Vanessa cardui). The annotation was used to identify expanded gene families, providing insight into the genetic underpinnings of this unique life-history. Here, I also developed linkage maps confirming a well-preserved karyotype in this species and showed that chromosome size is a major determinant of the recombination landscape. In Chapter IV, I explored the relationship between nucleotide composition, codon usage, and substitution rates across multiple Lepidoptera species, in an attempt to disentangle the relative effects of natural selection and neutral evolutionary forces on gene sequence evolution. The final two chapters focus on understanding the genetic basis of key adaptive traits in butterflies. Specifically, in Chapter V, I investigated potential local adaption in Leptidea sinapis by studying how host plant switch is associated with oviposition rates, larval growth and development, gene expression, and microbiome composition in populations experiencing different environmental conditions. In Chapter VI, I assessed the differential activation of regulatory elements in V. cardui females in response to host plant availability, which together with the gene family analysis in Chapter III, resulted in a set of candidate genes potentially associated with a migratory lifestyle. In conclusion, I have explored the complex interplay between proximate mechanisms and evolutionary forces shaping the genome structure and levels of genetic variation. I also investigated the genetic and regulatory underpinnings of adaptive traits in different butterfly species. In addition, I provided resources including chromosome-level genome assemblies, recombination maps, and annotations that will contribute to our understanding of evolutionary processes in general. 

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