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

Abstract

Phenotypic convergence, describing the independent evolution of similar characteristics, offers unique insights into how natural selection influences developmental and molecular processes to generate shared adaptations. The extinct marsupial thylacine and placental gray wolf represent one of the most extraordinary cases of convergent evolution in mammals, sharing striking cranial similarities despite 160 million years of independent evolution. We digitally reconstructed their cranial ontogeny from birth to adulthood to examine how and when convergence arises through patterns of allometry, mosaicism, modularity, and integration. We find the thylacine and wolf crania develop along nearly parallel growth trajectories, despite lineage-specific constraints and heterochrony in timing of ossification. These constraints were found to enforce distinct cranial modularity and integration patterns during development, which were unable to explain their adult convergence. Instead, we identify a developmental origin for their convergent cranial morphologies through patterns of mosaic evolution, occurring within bone groups sharing conserved embryonic tissue origins. Interestingly, these patterns are accompanied by homoplasy in gene regulatory networks associated with neural crest cells, critical for skull patterning. Together, our findings establish empirical links between adaptive phenotypic and genotypic convergence and provides a digital resource for further investigations into the developmental basis of mammalian evolution.

A Chromosome-Scale Hybrid Genome Assembly of the Extinct Tasmanian Tiger (Thylacinus cynocephalus)

“…These groups contain numerous species of significant interest to the fields of evolutionary, developmental, and conservation biology, such as the Tasmanian devil, quolls, dunnarts, and the numbat ( Fancourt 2016 ; Spencer et al 2020 ; Wright et al 2020 ; Cook et al 2021 ; Stahlke et al 2021 ). Moreover, the thylacine's exceptional craniofacial similarities with canids, despite their ∼160 Myr divergence, make the species an excellent model system to study the genomic basis of morphological evolution ( Bininda-Emonds et al 2007 ; Feigin et al 2018 ; Newton et al 2021 ; Rovinsky et al 2021 ). Improved genomic resources for this species are thus of considerable value to the broader genomics community.…”

A chromosome-scale hybrid genome assembly of the extinct Tasmanian tiger (Thylacinus cynocephalus)

“…Moreover, the thylacine's exceptional craniofacial similarities with canids, despite their ~160 million year divergence, make the species an excellent model system to study the genomic basis of morphological evolution (Bininda-Emonds, et al 2007;Feigin, et al 2018;Newton, et al 2021;Rovinsky, et al 2021). Improved genomic resources for this species are thus of considerable value to the broader genomics community.…”

“…These groups contain numerous species of significant interest to evolutionary, developmental and conservation biology, such as the Tasmanian devil, quolls, dunnarts and the numbat (Cook, et al 2021; Fancourt 2016; Spencer, et al 2020; Stahlke, et al 2021; Wright, et al 2020). Moreover, the thylacine’s exceptional craniofacial similarities with canids, despite their ~160 million year divergence, make the species an excellent model system to study the genomic basis of morphological evolution (Bininda-Emonds, et al 2007; Feigin, et al 2018; Newton, et al 2021; Rovinsky, et al 2021). Improved genomic resources for this species are thus of considerable value to the broader genomics community.…”

Morphometric and Genetic Description of Trophic Adaptations in Cichlid Fishes

“…Previous analysis of the strengths and patterns of covariation (i.e., modularity) in cichlid craniofacial structures [ 52 ] found that the pre-orbital and post-orbital regions act as independent modules. However, studies in mammals, birds, and the Archosaur group have identified modularity within the skull based on developmental origins [ 53 , 54 , 55 ] or function and articulation [ 54 , 56 ]. A full understanding of the patterns of morphological variation, as well as the number and effects of genes that underlie these shapes, is necessary to clarify which aspects of head anatomy demonstrate covariation, have increased evolutionary flexibility, or are simpler versus more complex phenotypes.…”