Abstract
Developmental constraints can have significant influence on the magnitude and direction of evolutionary change, and many studies have demonstrated that these effects are manifested on macroevolutionary scales. Phenotypic integration, or the strong interactions among traits, has been similarly invoked as a major influence on morphological variation, and many studies have demonstrated that trait integration changes through ontogeny, in many cases decreasing with age. Here, we unify these perspectives in a case study of the ontogeny of the mammalian cranium, focusing on a comparison between marsupials and placentals. Marsupials are born at an extremely altricial state, requiring, in most cases, the use of the forelimbs to climb to the pouch, and, in all cases, an extended period of continuous suckling, during which most of their development occurs. Previous work has shown that marsupials are less disparate in adult cranial form than are placentals, particularly in the oral apparatus, and in forelimb ontogeny and adult morphology, presumably due to functional selection pressures on these two systems during early postnatal development. Using phenotypic trajectory analysis to quantify prenatal and early postnatal cranial ontogeny in 10 species of therian mammals, we demonstrate that this pattern of limited variation is also apparent in the development of the oral apparatus of marsupials, relative to placentals, but not in the skull more generally. Combined with the observation that marsupials show extremely high integration of the oral apparatus in early postnatal ontogeny, while other cranial regions show similar levels of integration to that observed in placentals, we suggest that high integration may compound the effects of the functional constraints for continuous suckling to ultimately limit the ontogenetic and adult disparity of the marsupial oral apparatus throughout their evolutionary history.
Highlights
Why some clades achieve immense taxonomic, morphological, or ecological diversity while other, often closely related, clades are modest or poor in some or all of these measures is a question that has interested evolutionary biologists for centuries
As large sample sizes for well-staged non-model organisms are difficult to obtain, it is not possible to ascertain if this pattern applies to other marsupials, but we suggested that this high integration of the oral apparatus early in postnatal ontogeny may reflect the need for strong coordination of these elements during a period when marsupial young are suckling constantly or near-constantly
PCO1 appeared to be dominated by overall size, with smallest or youngest specimens falling at the negative end of the PCO1, while the largest and oldest specimens were directed toward the positive end of that axis (Fig. 3A)
Summary
Why some clades achieve immense taxonomic, morphological, or ecological diversity while other, often closely related, clades are modest or poor in some or all of these measures is a question that has interested evolutionary biologists for centuries. Attempts to understand this phenomenon can focus either on the successful clade, perhaps identifying a key innovation or new opportunity that allowed for its radiation, or on the depauperate one, testing for evidence of a developmental constraint or lack of ecological opportunity that has limited its ability to evolve as quickly or as much.
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