Interplay of genetic and epigenetic variation in evolutionary processes

Merondun, Justin (2024): Interplay of genetic and epigenetic variation in evolutionary processes. Dissertation, LMU München: Fakultät für Biologie

Abstract

Adaptation and speciation are the fundamental processes shaping the biodiversity that surrounds us. The Modern Evolutionary Synthesis, merging Darwinian theory with Mendelian principles, requires an understanding of the genetic and epigenetic contributions to population divergence across micro- and macro-evolutionary scales to explain the maintenance of biodiversity. This dissertation examines the interplay of genetic and epigenetic variation with relevance to evolution across the dimensions of wild avian populations, sexes, and species. Utilizing natural variation in two avian systems, the scope of my investigation extends to: 1) the genetic architecture sustaining female-limited polymorphism in cuckoos, the 2) evolutionary maintenance of mimetic egg phenotypes and host specialization in cuckoos, the 3) the epigenetic factors regulating dosage compensation and dosage balance in crows, and 4) the relevance of DNA methylation to speciation in crows. In paper I, together with my colleagues I identify the genetic basis and evolutionary maintenance of a female-limited plumage polymorphism. While all male common cuckoos are grey, females are either monochromatic grey or rufous. We found that plumage polymorphism maps to the female-restricted W chromosome, and that these ancient maternal haplotypes have been maintained after descent from a common ancestor in two cuckoo sister taxa, likely through balancing selection. Our findings suggest that genetic variation residing on sex-limited chromosomes can be a key determinant in the maintenance of trait variation across species boundaries. In paper II, I examine the genetic basis of host specialization and egg mimicry resulting from a co-evolutionary arms race. Common cuckoos are generalist obligate brood parasites exhibiting an extreme diversity of mimetic eggs which they use to exploit numerous hosts across Eurasia. I identified that matrilineal haplotypes are associated with mimetic egg phenotypes, and found that these haplotypes are maintained across the species’ range from the combinatorial effects of balancing selection and gene flow. I identify mitochondrial OXPHOS genes as the nexus of egg diversification, working in concert with nuclear and W-linked genes to provide a fast-evolving substrate to facilitate phenotypic innovation for new mimetic eggs while ensuring stable transmission of phenotypes from mothers to daughters. In paper III, together with colleagues I shed light on the mechanisms underlying dosage balance and compensation in a female heterogametic system in Eurasian crow. While male heterogametic systems often exhibit inactivation of a female homogametic chromosome, dosage balance in avian systems is less clear. We identified a significant correlation between the upregulation of female Z-linked genes and increased chromatin accessibility, which appears to be the key driver of dosage balance between the sexes. In contrast to other systems, 5mC methylation did not covary with dosage, underlining the importance of chromatin accessibility over methylation in regulating gene dosage in crows. In my last chapter, manuscript IV, examines the extent to which 5mC methylation contributes to nascent species divergence in Eurasian crows. Using genome and methylome sequencing data from all-black carrion crows, grey-coated hooded crows, and their hybrids, we found that taxon-related methylation divergence is restricted to intergenic space within the region of genetic differentiation responsible for plumage polymorphism. While epigenetic factors may aid in translating genetic variation to phenotype and largely coincide with the ontogenetic program, its autonomous contribution to evolution is minimal in this system. Collectively, these studies show the complex interplay of genetic and epigenetic factors contributing to the maintenance of evolutionary patterns. These findings add to our understanding of how epigenetic and genetic mechanisms cooperate to generate and maintain evolutionarily relevant phenotypes across populations and species, and break new ground by exploring the hitherto poorly explored dynamics of sex-limited chromosomes and the contributions of epigenetic variation to evolution.

• Dokumententyp: Dissertationen (Dissertation, LMU München)
• Keywords: Evolution, Genomics, Speciation, Epigenetics
• Themengebiete: 500 Naturwissenschaften und Mathematik ; 500 Naturwissenschaften und Mathematik > 570 Biowissenschaften, Biologie
• Fakultäten: Fakultät für Biologie
• Sprache der Hochschulschrift: Englisch
• Datum der mündlichen Prüfung: 13. Juni 2024
• 1. Bericht­erstatter:in: Wolf, Jochen B. W.