On the origins of phenotypic parallelism in benthic and limnetic stickleback

Dean, Laura L; Magalhaes, Isabel Santos; D’Agostino, Daniele; Hohenlohe, Paul; MacColl, Andrew D C

Abstract

Rapid evolution of similar phenotypes in similar environments, giving rise to in situ parallel adaptation, is an important hallmark of ecological speciation. However, what appears to be in situ adaptation can also arise by dispersal of divergent lineages from elsewhere. We test whether two contrasting phenotypes repeatedly evolved in parallel, or have a single origin, in an archetypal example of ecological adaptive radiation: benthic–limnetic three-spined stickleback (Gasterosteus aculeatus) across species pair and solitary lakes in British Columbia. We identify two genomic clusters across freshwater populations, which differ in benthic–limnetic divergent phenotypic traits and separate benthic from limnetic individuals in species pair lakes. Phylogenetic reconstruction and niche evolution modeling both suggest a single evolutionary origin for each of these clusters. We detected strong phylogenetic signal in benthic–limnetic divergent traits, suggesting that they are ancestrally retained. Accounting for ancestral state retention, we identify local adaptation of body armor due to the presence of an intraguild predator, the sculpin (Cottus asper), and environmental effects of lake depth and pH on body size. Taken together, our results imply a predominant role for retention of ancestral characteristics in driving trait distribution, with further selection imposed on some traits by environmental factors.

Citation

Dean, L. L., Magalhaes, I. S., D’Agostino, D., Hohenlohe, P., & MacColl, A. D. C. (2023). On the origins of phenotypic parallelism in benthic and limnetic stickleback. Molecular Biology and Evolution, 40(9), Article msad191. https://doi.org/10.1093/molbev/msad191

• Journal Article Type: Article
• Acceptance Date: Aug 16, 2023
• Online Publication Date: Aug 31, 2023
• Publication Date: 2023-09
• Deposit Date: Jan 21, 2024
• Publicly Available Date: Jan 31, 2024
• Journal: Molecular Biology and Evolution
• Print ISSN: 0737-4038
• Electronic ISSN: 1537-1719
• Publisher: Oxford University Press
• Peer Reviewed: Peer Reviewed
• Volume: 40
• Issue: 9
• Article Number: msad191
• DOI: https://doi.org/10.1093/molbev/msad191
• Keywords: Genetics; Molecular Biology; Ecology, Evolution, Behavior and Systematics
• Public URL: https://nottingham-repository.worktribe.com/output/24870049
• Publisher URL: https://academic.oup.com/mbe/article/40/9/msad191/7257493?login=false