The influence of divergent reproductive strategies in shaping modularity and morphological evolution in mammalian jaws

Abstract

Marsupial neonates are born at an earlier developmental stage than placental mammals, but the rapid development of their forelimbs and cranial skeleton allows them to climb to the pouch, begin suckling and complete their development ex utero. The mechanical environment in which marsupial neonates develop is vastly different from that of placental neonates, which exhibit a more protracted development of oral muscles and bones. This difference in reproductive strategy has been theorized to constrain morphological evolution in the oral region of marsupials. Here, we use 3D morphometrics to characterize one of these oral bones, the lower jaw (dentary), and assess modularity (pattern of covariation among traits), morphological disparity and rates of morphological evolution in two clades of carnivorous mammals: the marsupial Dasyuromorphia and placental fissiped Carnivora. We find that dasyuromorph dentaries have fewer modules than carnivorans and exhibit tight covariation between the angular and coronoid processes, the primary attachment sites for jaw‐closing muscles. This pattern of modularity may result from the uniform action of muscles on the developing mandible during suckling. Carnivorans are free from this constraint and exhibit a pattern of modularity that more strongly reflects genetic and developmental signals of trait covariation. Alongside differences in modularity, carnivorans exhibit greater disparity and faster rates of morphological evolution compared with dasyuromorphs. Taken together, this suggests dasyuromorphs have retained a signal of trait covariation that reflects the outsized influence of muscular force during early development, a feature that may have impacted the ability of marsupial carnivores to explore specialized regions of morphospace.

Correlated evolution of beak and braincase morphology is present only in select bird clades

“…Unlike previous studies using methodologies similar to ours that allow for direct comparisons of support for modularity hypotheses, we found little support for complex modularity scenarios. The discrepancy between this finding and that of , who suggested that the avian skull is defined by seven evolutionary modules may be explained by the aforementioned tendency of the maximum likelihood method used to favor more complex modularity hypotheses (Adams and Collyer, 2019), a finding that is echoed in research using this method (Goswami and Finarelli, 2016;Mitchell et al, 2021;Marshall et al, 2019;Conith et al, 2020Conith et al, , 2022Bardua et al, 2020). It is, however, notable that some authors (e.g.…”

Correlated evolution of beak and braincase morphology is present only in select bird clades

“…Unlike previous studies using methodologies similar to ours that allow for direct comparisons of support for modularity hypotheses, we found little support for complex modularity scenarios. The discrepancy between this finding and that of Felice and Goswami (2018), who suggested that the avian skull is defined by seven evolutionary modules may be explained by the aforementioned tendency of the maximum likelihood method used to favor more complex modularity hypotheses (Adams & Collyer, 2019), a finding that is echoed in research using this method (Bardua et al, 2020; Conith et al, 2020, 2022; Goswami & Finarelli, 2016; Marshall et al, 2019; Mitchell et al, 2021). It is, however, notable that some authors (e.g., Mitchell et al, 2021) have found consistent results between this maximum likelihood method and CR method, suggesting that in certain species a high number of semi‐independent modules may be a genuine pattern.…”

Functional constraints channel mandible shape ontogenies in rodents

“…However, early shape differentiation may have a profound effect on the directionality and intensity of shape changes through ontogenies. For instance, early functional requirements of the jaw or the forelimbs in relation to precocious suckling or crawling in marsupials have constrained the rate of shape evolution and disparity in comparison with eutherians [16][17][18][19].…”