Examples of convergent evolution, in which similar morphological, behavioral or functional traits arise independently in different species, provide a powerful framework for examining the extent to which the genetic changes underlying adaptive evolution are predictable versus idiosyncratic, a fundamental question in comparative genomics. Avian brood parasites, birds that provide no parental care to their offspring but instead lay their eggs in the nests of other species, represent an ideal model system for comparative analysis because brood parasitism (and the loss of parental care behavior) evolved independently seven times in five different avian families. This project will characterize patterns of genomic change in both parasitic and non-parasitic birds to test whether changes in the same specific genes and/or parallel patterns of genomic change have occurred in independent brood parasitic lineages. The results will also provide insight into other fundamental questions about genome evolution, including whether genetic changes underlying differences in behavior are most often in regulatory portions of the genome or represent structural changes to the genes themselves. In a second, related line of inquiry, the project will examine the unique evolutionary dynamics of the sex-determination chromosomes, leveraging recent research showing that specialized adaptations for exploiting particular host species are maternally inherited (passed from mother to daughter) and therefore encoded on the avian W-chromosome (analogous to the human Y-chromosome) in three different brood parasitic species. The project will also contribute to the training of scientists at various career stages including undergraduates, graduate students, and a postdoctoral fellow. A research experience for undergraduates (REU) component will provide an opportunity for two students from East Carolina University to receive training in bioinformatics at Harvard University. The project will produce high quality genome assemblies for additional bird species, supporting additional comparative analyses of genome evolution across vertebrates, and data from the project will be integrated into educational materials supporting courses in the emerging fields of molecular and population genomics.
Avian brood parasites and their hosts, which exhibit a spectacular diversity of behavioral, morphological and physiological adaptations and counter-adaptations, have served as important models for the study of coevolution. Recent discoveries of genetically divergent, host-specific matrilines within each of three different parasitic species, examples of "adaptation without recombination", present a unique opportunity to examine the effects of selection on the non-recombining, sex-limited chromosome. Likewise, with seven independent origins of obligate parasitism and associated loss of parental care, brood parasites offer an unparalleled opportunity to explore the genome-wide consequences of a major life history transition, providing greater power for tests of genomic convergence than in other recent analyses of the genomic basis of phenotypic convergence. Results of the study will lend insight into basic questions about genome evolution, including the relative importance of determinism versus historical contingency, and the manner in which integration versus modularity of genetic networks constrains the outcomes of natural selection. In addition to increasing the number of high quality genome assemblies for birds (currently available for only zebra finch and chicken) and assembling W-chromosome sequences, the proposed study will test two major hypotheses: 1) that evolutionary processes influencing the non-recombining, sex-limited W-chromosome (e.g., Hill-Robertson interference, selective sweeps, genetic hitchhiking) are amplified in parasitic lineages that have maternally inherited host-specific adaptations; and 2) examining all seven parasitic clades, that the evolution of brood parasitism (and loss of parental care behavior) results in genome-wide signatures of molecular convergence and/or convergent changes in coding and/or regulatory regions associated with particular genetic pathways or functions.
This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.