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

• Published in: Journal of evolutionary biology Vol. 35; no. 1; pp. 164 - 179
• Main Authors: Conith, Andrew J., Meagher, Molly A., Dumont, Elizabeth R.
• Format: Journal Article
• Language: English
• Published: Switzerland Blackwell Publishing Ltd 01-01-2022
• Subjects: Animals; Biological Evolution; Bones; Carnivores; constraints; Developmental stages; Divergence; Evolution; Female; Jaw; Mammals; Mammals - anatomy & histology; Mammals - genetics; Mandible; Marsupials; Modularity; morphological disparity; morphological rates; Morphology; Morphometry; Muscles; Neonates; Placenta; Pregnancy; Reproductive strategy; Suckling behavior; modularity; mammals; morphological disparity; constraints; morphological rates
• ISSN: 1010-061X; 1420-9101
• DOI: 10.1111/jeb.13944

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.
Marsupial and placental mammals exhibit very different modes of reproduction. 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. To assess how reproductive differences have impacted mammal evolution, we document the rate of morphological evolution, morphological disparity and the pattern of modularity in the mandible of the placental fissiped Carnivora and marsupial Dasyuromorphia. We find that the Carnivora exhibit faster rates, and greater disparity compared with the Dasyuromorphia, and the pattern of mandible modularity reflects a combination of cellular and biomechanical processes. The Dasyuromorphia, however, exhibit a pattern of modularity that primarily reflects only biomechanical processes, which likely results from the drastically different mechanical environment dasyuromorph neonates develop within.