Insights into the Speciation Process from Genomic and Phenotypic Analysis of an Avian Hybrid Zone in Amazonia

Abstract

Understanding the outcome of secondary contact is essential to shed light on the mechanisms governing species formation and maintenance. In Amazonia, closely related bird taxa with limited dispersal abilities are often separated by rivers, which presumably act as dispersal barriers. However, at the headwaters, rivers cease to be dispersal barriers, and this generates opportunities for secondary contact. In my dissertation, I studied genomic mechanisms associated with phenotypic differences, mitochondrial DNA structure, and putative reproductive barriers between two hybridizing Amazonian bird species in the genus Rhegmatorhina, a group of antbirds that find their arthropod prey exclusively by following army-ant swarms. Rhegmatorhina hoffmannsi occurs west of the Sucunduri River and R. berlepschi occurs east of the same river. Where the distributions of R. hoffmannsi and R. berlepschi meets along the Sucunduri’s headwaters, they form a hybrid zone, where birds with intermediate plumage can be found. In Chapter 1, I introduce the Rhegmatorhina genus, and list my general goals, such as describing Amazonian avian contact zones and exploring the genomic mechanisms contributing to their persistence. In Chapter 2, I present a description of genomic and phenotypic variation in the Rhegmatorhina hoffmannsi and R. berlepschi hybrid zone using RADseq data, one mitochondrial gene and spectrometry for plumage coloration. My results suggest little genetic differentiation between the two taxa, and displaced mitochondrial and nuclear geographic transitions in the system, with the Aripuanã, a river 120 km south of the Sucunduri, being the barrier between mitochondrial haplogroups. In Chapter 3, I sequenced a reference genome of R. hoffmannsi (PacBio and Hi-C assembly) and produced resequencing data for 81 individuals spanning the Rhegmatorhina hybrid zone to look for genomic regions possibly associated with plumage color and reproductive barriers. I found at least three chromosomal inversions and two candidate genes affecting plumage color (the genes TYR and TYRP1). Single nucleotide polymorphisms (SNPs) under significant selective pressure indicate a role for post-zygotic reproductive barriers (chromosomal inversions) and pre-zygotic barriers (plumage color differences) in the maintenance of the Rhegmatorhina hybrid zone. In Chapter 4, I examine whether mitochondrial and nuclear clines are displaced across the Rhegmatorhina hybrid zone, and I explore whether mitonuclear incompatibilities could be playing a role in the maintenance of the Rhegmatorhina hybrid zone. The complete mitochondrial genomes revealed a previously unknown mitochondrial haplotype that transitions in the same area as the plumage and nuclear clines, indicating that nuclear and mitochondrial clines are not displaced. Our results emphasize the importance of full mitochondrial genomes to describe mitochondrial genetic structure in contact zones. The genome-wide association analysis indicated no role of mitonuclear incompatibilities in the maintenance of the Rhegmatorhina hybrid zone, but did indicate a candidate nuclear gene that may be involved in a mitonuclear interaction between the two mitochondrial lineages of hoffmannsi separated by the Aripuanã River. In Chapter 5, I transition from the Rhegmatorhina system to describe the results of field work along the Juruá River. During the Emilie Snethlage Expedition, I found evidence for distributional turnovers across the Juruá River for four bird taxon pairs, suggesting the existence of avian contact zones at the Juruá River headwaters. In Chapter 6, I summarize the major results obtained in my dissertation, emphasizing how they add to our understanding of the roles of phenotypic and genomic differentiation in the outcome of secondary contact.