Abstract

The Tasmanian tiger or thylacine (Thylacinus cynocephalus) was the largest carnivorous Australian marsupial to survive into the modern era. Despite last sharing a common ancestor with the eutherian canids ~160 million years ago, their phenotypic resemblance is considered the most striking example of convergent evolution in mammals. The last known thylacine died in captivity in 1936 and many aspects of the evolutionary history of this unique marsupial apex predator remain unknown. Here we have sequenced the genome of a preserved thylacine pouch young specimen to clarify the phylogenetic position of the thylacine within the carnivorous marsupials, reconstruct its historical demography and examine the genetic basis of its convergence with canids. Retroposon insertion patterns placed the thylacine as the basal lineage in Dasyuromorphia and suggest incomplete lineage sorting in early dasyuromorphs. Demographic analysis indicated a long-term decline in genetic diversity starting well before the arrival of humans in Australia. In spite of their extraordinary phenotypic convergence, comparative genomic analyses demonstrated that amino acid homoplasies between the thylacine and canids are largely consistent with neutral evolution. Furthermore, the genes and pathways targeted by positive selection differ markedly between these species. Together, these findings support models of adaptive convergence driven primarily by cis-regulatory evolution.

Highlights

  • The Tasmanian tiger or thylacine (Thylacinus cynocephalus) was the largest carnivorous Australian marsupial to survive into the modern era

  • The thylacine’s extinction and the resulting paucity of molecular data has far prevented analyses that could clarify the genetic basis of this adaptive phenotypic convergence

  • We assessed the quality of the data by mapping reads to the genome of the Tasmanian devil (Sarcophilus harrisii)[10], the most closely related species available

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Summary

Results and discussion

The prevalence of homoplasy between the thylacine and canids did not defy expectations based on neutral evolution and was comparable to pairwise comparisons between non-convergent species with similar phylogenetic distances (Fig. 4 and Supplementary Table 10). Despite the slightly smaller number of positively selected genes identified in the Tasmanian devil and Bovidae (209 and 40 genes, respectively; Supplementary Tables 16 and 17), this comparison returned five overlapping genes, nearly the same number observed between thylacine and canids (Supplementary Table 18) From this we concluded that positive selection has not targeted orthologous genes more frequently in the thylacine and canids than in non-convergent species with similar divergence times. Our data demonstrate that observed amino acid homoplasies between thylacine and canid orthologous protein-coding genes are largely consistent with neutral evolutionary processes Such molecular changes are unlikely to explain the convergent phenotypes between these species. We suggest that future genome-wide studies on the molecular basis of convergent phenotypic evolution should explore the contribution of cis-regulatory changes to this phenomenon

Methods
Statistical parameters
Antibodies
Full Text
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