Incomplete lineage sorting and phenotypic evolution in marsupials

Incomplete lineage sorting (ILS) makes ancestral genetic polymorphisms persist during rapid speciation events, inducing incongruences between gene trees and species trees. ILS has complicated phylogenetic inference in many lineages, including hominids. However, we lack empirical evidence that ILS leads to incongruent phenotypic variation. Here, we performed phylogenomic analyses to show that the South American monito del monte is the sister lineage of all Australian marsupials, although over 31% of its genome is closer to the Diprotodontia than to other Australian groups due to ILS during ancient radiation. Pervasive conflicting phylogenetic signals across the whole genome are consistent with some of the morphological variation among extant marsupials. We detected hundreds of genes that experienced stochastic fixation during ILS, encoding the same amino acids in non-sister species. Using functional experiments, we confirm how ILS may have directly contributed to hemiplasy in morphological traits that were established during rapid marsupial speciation ca. 60 mya.

Automated summary

Incomplete lineage sorting (ILS) can lead to incongruences between gene trees and species trees during rapid speciation events. Through phylogenomic analyses, it has been discovered that the South American monito del monte is the sister lineage of all Australian marsupials, despite a portion of its genome being more similar to the Diprotodontia. Conflicting phylogenetic signals across the whole genome are consistent with morphological variation among extant marsupials. Furthermore, hundreds of genes have been found to encode the same amino acids in non-sister species due to stochastic fixation during ILS. Functional experiments have provided evidence of how ILS directly contributes to hemiplasy in morphological traits established during rapid marsupial speciation approximately 60 million years ago.