Comparative genomics uncovers the evolutionary history, demography, and molecular adaptations of South American canids

The remarkable radiation of South American (SA) canids produced 10 extant species distributed across diverse habitats, including disparate forms such as the short-legged, hypercarnivorous bush dog and the long-legged, largely frugivorous maned wolf. Despite considerable research spanning nearly two centuries, many aspects of their evolutionary history remain unknown. Here, we analyzed 31 whole genomes encompassing all extant SA canid species to assess phylogenetic relationships, interspecific hybridization, historical demography, current genetic diversity, and the molecular bases of adaptations in the bush dog and maned wolf. We found that SA canids originated from a single ancestor that colonized South America 3.9 to 3.5 Mya, followed by diversification east of the Andes and then a single colonization event and radiation of Lycalopex species west of the Andes. We detected extensive historical gene flow between recently diverged lineages and observed distinct patterns of genomic diversity and demographic history in SA canids, likely induced by past climatic cycles compounded by human-induced population declines. Genome-wide scans of selection showed that disparate limb proportions in the bush dog and maned wolf may derive from mutations in genes regulating chondrocyte proliferation and enlargement. Further, frugivory in the maned wolf may have been enabled by variants in genes associated with energy intake from short-chain fatty acids. In contrast, unique genetic variants detected in the bush dog may underlie interdigital webbing and dental adaptations for hypercarnivory. Our analyses shed light on the evolution of a unique carnivoran radiation and how it was shaped by South American topography and climate change.

The de novo genome assemblies of the maned wolf and bush dog have been deposited in GenBank (https://www.ncbi.nlm.nih.gov) (115) under accessions JALPRZ000000000, version ChrBra_1.0 (https://www.ncbi.nlm.nih.gov/nuccore/JALPRZ000000000.1/), and JALPSA000000000 version SpeVena.1.0 (https://www.ncbi.nlm.nih.gov/nuccore/JALPSA000000000.1/) (116), respectively. The raw sequencing reads of the South American canid taxa generated for this study are available under BioProject PRJNA822671 (https://www.ncbi.nlm.nih.gov/search/all/?term=PRJNA822671) (117). Genomes from other canid taxa were obtained from previous publications and are available on NCBI (see Table S1 for accession numbers). The scripts used in this work are available on Github (https://github.com/dechavezv/2nd.paper.v2) (118).

Previously published data were used for this work:(119), (120), (121), (122), (123), (124), (125), (126), (127), and (128).