Flexible conservatism in the skull modularity of convergently evolved myrmecophagous placental mammals

The skull of placental mammals constitutes one of the best studied systems for phenotypic modularity. Several studies have found strong evidence for the conserved presence of two- and six-module architectures, while the strength of trait correlations (integration) has been associated with major developmental processes such as somatic growth, muscle-bone interactions, and tooth eruption. Among placentals, ant- and termite-eating (myrmecophagy) represents an exemplar case of dietary convergence, accompanied by the selection of several cranial morphofunctional traits such as rostrum elongation, tooth loss, and mastication loss. Despite such drastic functional modifications, the covariance patterns of the skull of convergently evolved myrmecophagous placentals are yet to be studied in order to assess the potential consequences of this dietary shift on cranial modularity.

Here, we performed a landmark-based morphometric analysis of cranial covariance patterns in 13 species of myrmecophagous placentals. Our analyses reveal that most myrmecophagous species present skulls divided into six to seven modules (depending on the confirmatory method used), with architectures similar to those of non-myrmecophagous placentals (therian six modules). Within-module integration is also similar to what was previously described for other placentals, suggesting that most covariance-generating processes are conserved across the clade. Nevertheless, we show that extreme rostrum elongation and tooth loss in myrmecophagid anteaters have resulted in a shift in intermodule correlations in the proximal region of the rostrum. Namely, the naso-frontal and maxillo-palatine regions are strongly correlated with the oro-nasal module, suggesting an integrated rostrum conserved from pre-natal developmental processes. In contrast, the similarly toothless pangolins show a weaker correlation between the anterior rostral modules, resembling the pattern of toothed placentals.

These results reveal that despite some integration shifts related to extreme functional and morphological features of myrmecophagous skulls, cranial modular architectures have conserved the typical mammalian scheme.