Conservation genomics and the evolution of the widespread endangered bunting species

Abstract

Population declines can reduce genetic diversity and lead to increased inbreeding and inbreeding depression due to deleterious mutations. These genetic features are influenced by demographic history, bottlenecks, and natural selection. Understanding the interaction of different processes is crucial for effective conservation management of endangered species. Small populations often receive more conservation attention due to genetic vulnerability. However, large populations, despite their essential role in maintaining ecosystem stability, are often overlooked and can also be at risk of extinction. In this thesis, I investigated the effects of these processes on genetic features of three widespread Old World bunting species - the Critically Endangered yellow-breasted bunting (Emberiza aureola), the Vulnerable rustic bunting (E. rustica), and the Least Concern little bunting (E. pusilla) - with similar distribution ranges, using whole-genome resequencing data. In Chapter 2, I aim to address the genetic threats faced by yellow-breasted bunting and its evolutionary potential. I found three populations of this species with shallow genetic differentiation and observed gene flow between these populations. These populations underwent similar population fluctuations in the past but differed in the extent of population decline, resulting in differences in genetic diversity, inbreeding, and deleterious mutations. My findings indicate that before the recent population collapse, the yellow-breasted bunting population exhibited relatively low genetic threats and displayed high evolutionary potential. However, the island population faced more significant genetic threats than other populations. In Chapter 3, I used empirical data from three bunting species alongside simulations to explore the genetic consequences of demographic history, bottlenecks, and natural selection. I found that the ancestral population size mainly determined genome-wide genetic diversity and the number of deleterious mutations, with the intensity of bottlenecks impacting the loss of genetic diversity and the accumulation and purging of deleterious mutations. Furthermore, the genetic diversity did not show significant recovery even after the population rebounded. In contrast, inbreeding was primarily influenced by the intensity of bottlenecks. Additionally, both runs of homozygosity and recombination impact the distribution of deleterious mutations across the genome, with these two factors interacting. In Chapter 4, I investigated genetic differentiation using the bunting system to understand how various evolutionary forces shape the genomic landscape within and between species. I found that genes under positive selection could vary within one species during different evolutionary periods. The genomic landscape between the three species pairs was predominantly shaped by gene flow, recombination, and linked selection, while recurrent selection, recombination, and linked selection played a significant role in shaping the genomic landscape between the population pairs of yellow-breasted bunting. In summary, this study advances our comprehension of the interplay of various evolutionary processes and their impacts on genetic diversity, inbreeding, and deleterious mutations. Furthermore, this study sheds light on the existence of multiple evolutionary models that shape genomic landscapes within a single system. Finally, I discussed the main determinants of these genetic features related to endangerment in Chapter 5. These findings are pivotal for effectively conserving endangered species, particularly those with large populations that have suffered from rapid declines in recent years.