Museum skins enable identification of introgression associated with cytonuclear discordance

Sally Potter; Craig Moritz; Maxine P Piggott; Jason G Bragg; Ana C Afonso Silva; Ke Bi; Christiana McDonald-Spicer; Rustamzhon Turakulov; Mark D B Eldridge

doi:10.1093/sysbio/syae016

Museum skins enable identification of introgression associated with cytonuclear discordance

Syst Biol. 2024 Apr 5:syae016. doi: 10.1093/sysbio/syae016. Online ahead of print.

Authors

Sally Potter^{1

2

3}, Craig Moritz², Maxine P Piggott^{2

4}, Jason G Bragg⁵, Ana C Afonso Silva⁶, Ke Bi⁷, Christiana McDonald-Spicer², Rustamzhon Turakulov⁸, Mark D B Eldridge³

Affiliations

¹ School of Natural Sciences, Macquarie University, Sydney, NSW, Australia.
² Division of Ecology and Evolution, Research School of Biology, The Australian National University, Acton, ACT, Australia.
³ Australian Museum Research Institute, Australian Museum, Sydney, NSW, Australia.
⁴ Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT, Australia.
⁵ National Herbarium of New South Wales, The Royal Botanical Gardens and Domain Trust, Sydney, NSW, Australia.
⁶ Univ. Lille, CNRS, UMR 8198 - Evo-Eco-Paleo, F-59000 Lille, France.
⁷ Museum of Vertebrate Zoology and Department of Integrative Biology, University of California Berkeley, Berkeley, California, United States of America.
⁸ The National Institutes of Health, Bethesda, Maryland, United States of America.

PMID: 38577768
DOI: 10.1093/sysbio/syae016

Abstract

Increased sampling of genomes and populations across closely related species has revealed that levels of genetic exchange during and after speciation are higher than previously thought. One obvious manifestation of such exchange is strong cytonuclear discordance, where the divergence in mitochondrial DNA (mtDNA) differs from that for nuclear genes more (or less) than expected from differences between mtDNA and nuclear DNA (nDNA) in population size and mutation rate. Given genome-scale datasets and coalescent modelling, we can now confidently identify cases of strong discordance and test specifically for historical or recent introgression as the cause. Using population sampling, combining exon capture data from historical museum specimens and recently collected tissues we showcase how genomic tools can resolve complex evolutionary histories in the brachyotis group of rock-wallabies (Petrogale). In particular, applying population and phylogenomic approaches we can assess the role of demographic processes in driving complex evolutionary patterns and assess a role of ancient introgression and hybridisation. We find that described species are well supported as monophyletic taxa for nDNA genes, but not for mtDNA, with cytonuclear discordance involving at least four operational taxonomic units (OTUs) across four species which diverged 183-278 kya. ABC modelling of nDNA gene trees supports introgression during or after speciation for some taxon pairs with cytonuclear discordance. Given substantial differences in body size between the species involved, this evidence for gene flow is surprising. Heterogenous patterns of introgression were identified but do not appear to be associated with chromosome differences between species. These and previous results suggest that dynamic past climates across the monsoonal tropics could have promoted reticulation among related species.

Keywords: cytonuclear discordance; exon capture; introgression; museum skins; rock-wallabies.