Widespread cis-regulatory convergence between the extinct Tasmanian tiger and gray wolf

Abstract

The extinct marsupial Tasmanian tiger, or thylacine, and the eutherian gray wolf are among the most widely recognized examples of convergent evolution in mammals. Despite being distantly related, these large predators independently evolved extremely similar craniofacial morphologies, and evidence suggests that they filled similar ecological niches. Previous analyses revealed little evidence of adaptive convergence between their protein-coding genes. Thus, the genetic basis of their convergence is still unclear. Here, we identified candidate craniofacial cis-regulatory elements across vertebrates and compared their evolutionary rates in the thylacine and wolf, revealing abundant signatures of convergent positive selection. Craniofacial thylacine-wolf accelerated regions were enriched near genes involved in TGF beta (TGFB) and BMP signaling, both of which are key morphological signaling pathways with critical roles in establishing the identities and boundaries between craniofacial tissues. Similarly, enhancers of genes involved in craniofacial nerve development showed convergent selection and involvement in these pathways. Taken together, these results suggest that adaptation in cis-regulators of TGF beta and BMP signaling may provide a mechanism to explain the coevolution of developmentally and functionally integrated craniofacial structures in these species. We also found that despite major structural differences in marsupial and eutherian brains, accelerated regions in both species were common near genes with roles in brain development. Our findings support the hypothesis that, relative to protein-coding genes, positive selection on cis-regulatory elements is likely to be an essential driver of adaptive convergent evolution and may underpin thylacine-wolf phenotypic similarities.

Ontogenetic origins of cranial convergence between the extinct marsupial thylacine and placental gray wolf

“…Here, adaptive molecular evolution may arise within FNP-NC and MES embryonic cell lineages, regulating the convergent development of these bone groups. This hypothesis is supported by the recent identification of thylacine-wolf homoplasy in gene-regulatory elements of major patterning genes and developmental pathways regulating cranial mesenchyme migration, differentiation, and ossification 48 . This is further supported where perturbations to patterning genes within cranial NC cells can directly alter facial morphology 24 .…”

“…We show that the cranial similarities between the thylacine and wolf are in fact mosaic 25 , where cranial bone groups with strong shape similarity arise from conserved embryological origins. Strikingly, these patterns are accompanied by genomic homoplasy within these key embryonic cell populations 48 , providing strong empirical links between phenotypic and genotypic homoplasy. These findings prompt exciting new research avenues to examine how molecular changes within tissue-specific regulatory networks may influence craniofacial shape disparity and convergence.…”

“…The extinct thylacine and gray wolf present an exceptional model of convergent evolution, with recent studies supporting extreme phenotypic similarity in the skull 7,9 and accompanying genomic homoplasy in craniofacial gene-regulatory elements 48 . However, the underlying developmental processes that link these homoplasies are not well understood.…”

“…Recent comparisons between the thylacine and wolf genomes 7 revealed extensive homoplasy in regulatory regions controlling craniofacial development 48 , suggesting the evolution of shared molecular pathways underlying their convergence. In this study, we further examine the developmental processes that have led to the extraordinary cranial convergence between the extinct thylacine and gray wolf 3,7 , building on a rare developmental series of thylacine pouch young 49 .…”

“…Using 3D landmark and point cloud-based geometric morphometric analyses, we examine the onset and extent of cranial similarity in ontogenetic and allometric growth patterns to determine how these are correlated throughout development. We specifically examine whether there is greater similarity between cranial regions with conserved embryonic tissue origins, linking phenotypic convergence with genetic homoplasy in craniofacial tissues 48 . In addition, we examine module covariation patterns between the thylacine and wolf throughout key stages of development, to determine whether their adaptive cranial shapes arise through homoplasious modularity and integration patterns.…”