Abstract
Adaptive radiations are characterized by the diversification and ecological differentiation of species, and replicated cases of this process provide natural experiments for understanding the repeatability and pace ofmolecular evolution.During adaptive radiation, genes related to ecological specialization may be subject to recurrent positive directional selection. However, it is not clear to what extent patterns of lineage-specific ecological specialization (includingphenotypic convergence) are correlatedwithsharedsignatures of molecular evolution. To test this, we sequenced whole exomes from a phylogenetically dispersed sample of 38 murine rodent species, a group characterized bymultiple, nested adaptive radiations comprising extensive ecological and phenotypic diversity.We found that genes associatedwithimmunity, reproduction, diet, digestion, and taste have been subject to pervasive positive selection during the diversification of murine rodents.We also found a significant correlation between genome-wide positive selection and dietary specialization, with a higher proportion of positively selected codon sites in derived dietary forms (i.e., carnivores and herbivores) than in ancestral forms (i.e., omnivores). Despite striking convergent evolution of skull morphology and dentition in two distantly related worm-eating specialists, we did not detect more genes with shared signatures of positive or relaxed selection than in a nonconvergent species comparison. Although a small number of the genes we detected can be incidentally linked to craniofacial morphology or diet, protein-coding regions are unlikely to be the primary genetic basis of this complex convergent phenotype.Our results suggest a linkbetween positive selection and derived ecological phenotypes, andhighlight specific genes and general functional categories that may have played an integral role in the extensive and rapid diversification of murine rodents.
| Original language | English |
|---|---|
| Article number | evab103 |
| Journal | Genome Biology and Evolution |
| Volume | 13 |
| Issue number | 7 |
| DOIs | |
| State | Published - Jul 1 2021 |
Funding
This study was supported by the U.S. Government National Science Foundation (grant numbers DEB-1457654, DEB-1754393, DEB-1754096, DEB-1441634, and OISE-0965856), National Institutes of Health (grant numbers R01-HD073439, R01-HD094787), National Geographic Society (9025-11), Australia and Pacific Science Foundation (12-6). E.R. was supported by an Australian Government Research Training Program Scholarship, the Dame Margaret Blackwood Soroptimist Scholarship and the Alfred Nicholas Fellowship. We are grateful to Gregg Thomas for providing feedback on an earlier version of this manuscript, Jonathan Nations for advice on murine trait data and comparative analyses, and comments from two anonymous reviewers that improved the final version. We are indebted to the Indonesian Institute of Sciences (Lembaga Ilmu Pengetahuan Indonesia, LIPI) for access to material from Sulawesi, and to Museums Victoria, the Australian Biological Tissue Collection, Louisiana State University Museum of Natural Science, University of Kansas Biodiversity Research Center, and the Field Museum of Natural History for access to specimens. We also thank Melbourne Bioinformatics and Research Platform Services at the University of Melbourne for access to high-performance computing resources.
| Funders | Funder number |
|---|---|
| OISE-0965856, DEB-1457654, DEB-1441634, DEB-1754096, DEB-1754393 | |
| R01-HD094787 | |
| R01HD073439 | |
| National Geographic Society | 9025-11 |
Keywords
- Murinae
- adaptive radiation
- comparative genomics
- convergent evolution
- exome capture
- positive selection