Reduced phenotypic covariation in marsupial limbs and the implications for mammalian evolution

Abstract

As serially homologous structures, mammalian fore-and hindlimbs ancestrally share a common developmental and genetic architecture. As a result, mammalian fore-and hindlimbs are predicted to be highly integrated in the absence of selective pressures to form divergent limb morphologies. Marsupials experience such a divergent selective pressure to form a robust forelimb to power a post-natal crawl to the teat. In this study, phenotypic covariation in marsupials was assessed to determine if specialization for the crawl did indeed reduce integration between their fore-and hindlimbs. To explore the evolution of mammalian limb integration, phenotypic covariation in representative eutherians and monotremes was also examined. Phenotypic covariation in limbs was quantified morphometrically, and analysed with correlational and phylogenetic methods. Results indicate that marsupials generally have relatively high levels of within-limb phenotypic covariation, and low levels between limbs, in contrast to the pattern reconstructed for the mammalian ancestor. Our findings support the hypothesis that pressure to specialize in one limb (either the fore-or the hindlimb) can reduce phenotypic covariation between limbs, and that reduced limb phenotypic covariation is derived in marsupials. Further research is needed to test the effect that these differences in limb phenotypic covariation had on the evolution of the major mammalian groups.

The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

“…Reconstructing Deep-Time Evolutionary Development Through Analysis of Phenotypic Integration in Fossils Recent studies linking shifts in phenotypic integration to differences in development among major clades have raised the exciting prospect of reconstructing developmental patterns from adult fossil specimens, potentially illuminating the often obscure biology of stem representatives for living clades (24)(25)(26). For example, the three major clades of extant mammals, placentals, marsupials, and monotremes, are characterized by markedly different developmental strategies that are reflected in wellstudied heterochronies in limb ossification.…”

“…In contrast, marsupials, pouched mammals with short intrauterine gestation periods and a requisite crawl to the pouch where highly altricial young undergo most of their development, show the opposite pattern. Foreand hindlimbs show strong integration within each limb, but weak or no integration across the limbs (24,26,38). Different again are the placental mammals, which show strong within-limb and between-limb integration, reflecting both functional associations and serial homology (28).…”

“…Much recent work has focused on characterizing large-scale patterns of trait relationships through comparative studies of extant and fossil taxa (11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23), in some cases demonstrating shifts in phenotypic integration related to changes in development (24)(25)(26), function (27)(28)(29), and environment (30)(31)(32)(33). Although focused overwhelmingly on model organisms, these studies provide a foundation for understanding how phenotypic integration changes through ontogenetic and evolutionary time and how it relates to myriad factors shaping morphological evolution.…”

Ecomorphological determinations in the absence of living analogues: the predatory behavior of the marsupial lion (Thylacoleo carnifex) as revealed by elbow joint morphology

“…! placentals in their ontogeny (Kelly and Sears 2011): marsupials are born in a highly altricial state and require well-developed forelimbs to climb to the mother's teat (Sears 2004 The elbow shape of Thylacoleo clusters in an intermediate position between that of highly arboreal placentals (i.e., primates and pilosans) and marsupials (i.e., phalangeroids and tree kangaroos). !Note, however, that Thylacoleo does not cluster with the arboreal marsupials: its scores on PC1 are similar to the wombat (Vombatus ursinus), the only terrestrial quadrupedal diprotodontid marsupial, and its scores on PC2 are more negative than any marsupial except the mountain cuscus (Phalanger carmelitae).…”

Statistical support for the hypothesis of developmental constraint in marsupial skull evolution

“…In a study quantifying ontogenetic changes in the shoulder girdle and comparing adult diversity in the scapula and pelvis, Sears [15] found evidence for constraint in marsupial shoulder-girdle morphology produced by this early functional requirement. There is also evidence that the early crawl constrains forelimb morphology in marsupials [16,17]. …”