A tree of geese: A phylogenomic perspective on the evolutionary history of True Geese

Abstract

Phylogenetic incongruence can be caused by analytical shortcomings or can be the result of biological processes, such as hybridization, incomplete lineage sorting and gene duplication. Differentiation between these causes of incongruence is essential to unravel complex speciation and diversification events. The phylogeny of the True Geese (tribe Anserini, Anatidae, Anseriformes) was, until now, contentious, i.e., the phylogenetic relationships and the timing of divergence between the different goose species could not be fully resolved. We sequenced nineteen goose genomes (representing seventeen species of which three subspecies of the Brent Goose, Branta bernicla) and used an exon-based phylogenomic approach (41,736 exons, representing 5887 genes) to unravel the evolutionary history of this bird group. We thereby provide general guidance on the combination of whole genome evolutionary analyses and analytical tools for such cases where previous attempts to resolve the phylogenetic history of several taxa could not be unravelled. Identical topologies were obtained using either a concatenation (based upon an alignment of 6,630,626 base pairs) or a coalescent-based consensus method. Two major lineages, corresponding to the genera Anser and Branta, were strongly supported. Within the Branta lineage, the White-cheeked Geese form a well-supported sub-lineage that is sister to the Red-breasted Goose (Branta ruficollis). In addition, two main clades of Anser species could be identified, the White Geese and the Grey Geese. The results from the consensus method suggest that the diversification of the genus Anser is heavily influenced by rapid speciation and by hybridization, which may explain the failure of previous studies to resolve the phylogenetic relationships within this genus. The majority of speciation events took place in the late Pliocene and early Pleistocene (between 4 and 2millionyears ago), conceivably driven by a global cooling trend that led to the establishment of a circumpolar tundra belt and the emergence of temperate grasslands. Our approach will be a fruitful strategy for resolving many other complex evolutionary histories at the level of genera, species, and subspecies.

Keywords: Concatenation; Consensus; Gene tree; Hybridization; Incomplete lineage sorting; Species tree.