Speciation Genomics in Australian Meliphagoid Birds

Abstract

The speciation process proceeds through a continuum of increasing genomic divergence and decreasing gene flow between populations. While sampling across hybrid zones provide insight for an intermediate stage of speciation, comparative studies of multiple contact zones between populations at different stages of speciation would expand our broader understanding of the process itself. Suture zones provide this ideal framework in a shared geographic context. For my thesis, I developed and utilized a suture zone system situated in northeastern Australia. From the array of contact zones in the region, I focused on species within the species-rich bird superfamily Meliphagoidea comprising the honeyeaters, fairywrens, gerygones, and allies. Using a comparative genomics approach, I tested hypotheses on how genome divergence and gene flow changes as populations diverge and proceed through the speciation process. The first chapter sets the stage for analyzing this new system. I characterized variation in genetic and morphological divergence across 27 meliphagoid species through three transition zones that comprise the system. Among factors that may predict genetic divergence, I found that taxonomic ranking outperforms morphological divergence and habitat preference. Establishing variation in divergence laid out a starting point for comparative study of gene flow, divergence, and speciation. The second chapter determines how well current geography predicts probability of gene flow during population divergence and speciation. From the initial set of species, I selected eight that are codistributed in four regions divided by known biogeographical barriers in northern Australia and Papua New Guinea. I found that historical connectivity between populations is a better predictor for likelihood of gene flow compared to current designations of allopatry or parapatry. Furthermore, this likelihood of gene flow decreases in a rapid, snowballing manner with increasing divergence in these populations. The third chapter characterizes how the geographic extent of gene flow changes with increasing divergence. From the initial set of species, I selected those involved in ten contact zones between parental population pairs in which divergence levels span the speciation continuum. I found that the cline widths across the contact zones decrease exponentially with increasing divergence of the parental populations. Furthermore, this width is correlated with the geographic range width in the contact zone, emphasizing the role of geographic range during speciation. The fourth and final chapter addresses the role of chromosomal rearrangements in speciation by characterizing inversions across the avian tree. Using a hybrid approach and a genetic linkage map, I sequenced and assembled a chromosome-scale reference genome for the superb fairywren (Malurus cyaneus) which fills a phylogenetic gap in existing avian genome assemblies. By comparing this assembly to other existing assemblies, I found novel fusions in the superb fairywren, confirmed the variation in inversions between autosomes and the Z chromosome, and revealed that inversions are much more prevalent in oscines than their nonpasserine counterparts. In this thesis, I developed and utilized a new system to take a comparative approach in speciation genomics. The conclusions emphasize the role of the context of geography and genome architecture on the rapid decrease of gene flow and accumulation of divergence during the speciation process. Show more