Throughout their evolutionary histories, marsupial mammals have been taxonomically and morphologically less diverse than their sister taxa the placentals. Because of this, it has been proposed that the evolution of marsupials has been constrained by the functional requirements of their mode of reproduction. Marsupials give birth after short gestation times to immature neonates that immediately crawl, under the power of their precociously developed shoulder girdles, to the teat where they attach and complete their early development. Using a novel approach incorporating adult and embryological morphological data, this study is the first to both: (1) statistically support adult patterns of morphological divergence consistent with the constraint hypothesis, and (2) identify ontogenetic patterns of morphological change that demonstrate that the constraint was responsible, at least in part, for their formation. As predicted by the marsupial constraint, the shoulder girdles of adult marsupials are less diverse than those of adult placentals, and adult marsupial scapulae are less morphologically diverse than adult marsupial pelves. Furthermore, marsupials that complete an extensive crawl to the teat are restricted to a common pattern of ontogenetic scapular shape change, strongly supporting the hypothesis that the morphological development of the marsupial scapula has been limited evolutionarily by its obligate role in the crawl to the teat. Because this study establishes that ontogenetic and evolutionary morphological change is correlated within mammalian scapulae, it is probable that the marsupial constraint also restricted the morphological divergence of the scapula over evolutionary time by limiting ontogenetic change in the scapula. These findings, coupled with the importance of the shoulder girdle in mammalian locomotor specialization, support the conclusion that the low morphological diversity of marsupial forms over evolutionary time could be directly due to the constraint on marsupial morphological evolution caused by the functional requirements of the crawl to the teat.
Diversification and adaptive radiations are tied to evolvability, which in turn is linked to morphological integration. Tightly integrated structures typically evolve in unison, whereas loosely integrated structures evolve separately. Highly integrated structures are therefore thought to constrain evolutionary change by limiting morphological disparity. Mounting evidence suggests that high integration may facilitate evolutionary change along a single trajectory. We used geometric morphometrics to compare cranial disparity and integration among phyllostomid bats-which exhibit the greatest dietary diversity of any mammalian family-and their sister taxa within the superfamily Noctilionoidea. Our results reveal that phyllostomids are more tightly integrated and have less disparity in cranial shape than their outgroups, despite exhibiting tenfold higher species richness and significantly increased rates of speciation. Phyllostomid cranial morphology appears to have diverged from that of other noctilionoids by evolving along a single axis of morphological variation that describes the relative length of the rostrum. We propose that phyllostomids were able to evolve to occupy a wide range of dietary niches by varying rostrum length, possibly along a line of least evolutionary resistance. This study provides a compelling empirical example of how increased integration can lead to adaptation, implying that both high and low integration can underlie diverse phenotypes in adaptive radiation.
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