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Download File Natural selection and demography shape the genomes of New World birds Lucas Rocha Moreira Submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy under the Executive Committee of the Graduate School of Arts and Sciences COLUMBIA UNIVERSITY 2021 © 2021 Lucas Rocha Moreira All Rights Reserved Abstract Natural selection and demography shape the genomes of New World birds Lucas Rocha Moreira Genomic diversity is shaped by the interplay between mutation, genetic drift, recombination, and natural selection. A major goal of evolutionary biology is to understand the relative contribution of these different microevolutionary forces to patterns of genetic variation both within and across species. The advent of massive parallel sequencing technologies opened new avenues to investigate the extent to which alternative evolutionary mechanisms impact the genome and the footprints they leave. We can leverage genomic information to, for example, trace back the demographic trajectory of populations and to identify genomic regions underlying adaptive traits. In this disser- tation, I employ genomic data to explore the role of demography and natural selection in two New World bird systems distributed along steep environmental gradients: the Altamira Oriole (Icterus gularis), a Mesoamerican bird that exhibits large variation in body size across its range, and the Hairy and Downy woodpecker (Dryobates villosus and D. pubescens), two sympatric species whose phenotypes vary extensively in response to environments in North America. In Chapter 1, I combine ecological niche model, phenotypic and ddRAD sequencing data from several individuals of I. gularis to investigate which spatial processes best explain geographic variation in phenotypes and alleles: (i) isolation by distance, (ii) isolation by history or (iii) isolation by environment. I find that the pronounced genetic and phenotypic variation in I. gularis are only partially correlated and differ regarding spatial predictors. Whereas genomic variation is largely explained by historical barriers to gene flow (IBH), variation in body size can be best predicted by contemporary environmental heterogeneity (IBE), which is consistent with a pattern produced by either natural selection or environmental plasticity. In Chapter 2, I conduct whole genome resequencing on 140 individuals of Downy and Hairy Woodpecker from across North America to more explicitly elucidate the impact of demog- raphy and natural selection on the genome. I find that despite spatial congruence in allele frequen- cies, population structure in these two species has been produced at different temporal scales. Whereas Hairy Woodpeckers were isolated into two east-west glacial refugia, Downy woodpecker populations seem to have expanded from a single ancestral refugium. Demographic analyses sug- gest large variation in Ne over the past one million years in both Hairy and Downy Woodpeckers, with repeated episodes of bottleneck followed by population expansion, consistent with the onset of the climatic oscillations of the Pleistocene. Nucleotide diversity in both species was positively correlated with recombination rate and negatively correlated with gene density, suggesting the ef- fect of linked selection. The magnitude of this effect, however, seems to have been modulated by the individual demographic trajectory of populations and species. Nevertheless, patterns of nucle- otide diversity along the genome are highly correlated between Hairy and Downy Woodpecker, which may be attributed to pervasive selection acting on a conserved genomic landscape of re- combination. Finally, in Chapter 3, I use a suite of statistical methods to scan the genome of Hairy and Downy Woodpecker for signatures of natural selection associated with population-specific envi- ronmental differences. I test whether climatic adaptation was achieved through selection on the same loci in both species, which would indicate parallel genetic mechanisms for adaptation. I find limited evidence of genomic parallelism at the SNP level, but large parallelism at the gene level. Candidate genes were involved in a broad range of biological processes, including immune re- sponse, nutritional metabolism, mitochondrial respiration, and embryonic development. Lastly, I identify potential candidates for key phenotypic traits in Downy and Hairy Woodpecker, such as genes in the IGF signaling pathway, putatively linked to differences in body size, and the mela- noregulin gene (MREG), potentially involved in plumage variation. Together, these findings high- light the significant role of demography and natural selection in shaping genomic variation. Table of Contents List of Figures .............................................................................................................................................. v List of Tables ............................................................................................................................................. vii List of Supplemental Materials ............................................................................................................... viii Acknowledgements ......................................................................................................................................x Dedication .................................................................................................................................................. xii Chapter 1 ...................................................................................................................................................... 1 1.1. Abstract ............................................................................................................................................. 2 1.2. Introduction ..................................................................................................................................... 3 1.3. Materials and Methods ................................................................................................................... 7 1.3.1. Sampling and DNA extraction ............................................................................................... 7 1.3.2. Double-digest restriction site-associated DNA (ddRAD) sequencing ............................. 7 1.3.3. mtDNA dataset ........................................................................................................................ 7 1.3.4. Genetic structure ...................................................................................................................... 8 1.3.5. Demographic modeling ........................................................................................................... 9 1.3.6. Modeling contemporary and paleo-distributions .............................................................. 10 1.3.7. Quantifying phenotypic data from museum specimens ................................................... 12 1.3.8. Predictors of genetic and phenotypic differentiation ....................................................... 13 1.4. Results ............................................................................................................................................. 14 1.4.1. Characteristics of SNP dataset ............................................................................................. 14 1.4.2. Genetic structuring across lowland Middle America ........................................................ 15 i 1.4.3. Demographic history ............................................................................................................. 19 1.4.4. Patterns and correlates of phenotypic variation ................................................................ 21 1.4.5. Predictors of genetic and phenotypic differentiation ....................................................... 23 1.5. Discussion ...................................................................................................................................... 26 1.5.1. Phylogeographic structure is best explained by historical barriers ................................. 26 1.5.2. Patterns of phenotypic variation are best explained by environment ............................ 29 1.6. Conclusion ...................................................................................................................................... 31 1.7. Author contribution ...................................................................................................................... 32 1.8. References ...................................................................................................................................... 33 1.9. Supplemental Material .................................................................................................................. 46 Chapter 2 .................................................................................................................................................... 53 2.1. Abstract ........................................................................................................................................... 54 2.2. Introduction ................................................................................................................................... 55 2.3. Results ............................................................................................................................................. 58 2.3.1. Congruent population structure and genetic diversity
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