Abstract

The morphological interdependence of traits, or their integration, is commonly thought to influence their evolution. As such, study of morphological integration and the factors responsible for its generation form an important branch of the field of morphological evolution. However, most research to date on post-cranial morphological integration has focused on adult patterns of integration. This study investigates patterns of correlation (i.e., morphological integration) among skeletal elements of the fore- and hind limbs of developing marsupial and placental mammals. The goals of this study are to establish how patterns of limb integration vary over development in marsupials and placentals, and identify factors that are likely responsible for their generation. Our results indicate that although the overall pattern of correlation among limb elements is consistent with adult integration throughout mammalian development, correlations vary at the level of the individual element and stage. As a result, the relative integration among fore- and hind limb elements varies dynamically between stages during development in both marsupial and placental mammals. Therefore, adult integration studies of the limbs may not be indicative of developmental integration. Results are also consistent with integration during early limb development being more heavily influenced by genetic and developmental factors, and later by function. Additionally, results are generally consistent with a constraint on marsupial forelimb evolution caused by the functional requirements of the crawl to the teat that operates by limiting morphological variation before and at the time of birth, and not after.

Highlights

  • The evolution of morphology through the process of natural selection is dependent upon the existence and distribution of morphological variation among individuals

  • Matrix repeatability was moderately high for all species for all developmental stages. This suggests that the sampling restrictions caused by working on limited embryonic materials did not significantly bias the estimation of correlation matrices (T. vulpecula, n 1⁄4 6, PND2 1⁄4 0.82; T. vulpecula, n 1⁄4 6, PND18 1⁄4 0.82; M. musculus, n 1⁄4 21, E13.5 1⁄4 0.88; M. musculus, n 1⁄4 22, E15.5 1⁄4 0.87; M. musculus, n 1⁄4 21, E17.5 1⁄4 0.87; M. domestica, n 1⁄4 24, Stage 33 1⁄4 0.97; M. domestica, n 1⁄4 7, PND1 1⁄4 0.96; M. domestica, n 1⁄4 6, PND5 1⁄4 0.94)

  • Results of the matrix correlation analyses suggest that overall patterns of correlation among skeletal elements of the fore- and hind limbs are highly similar between the developmental stages examined in this study

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Summary

Introduction

The evolution of morphology through the process of natural selection is dependent upon the existence and distribution of morphological variation among individuals. Our understanding of the processes shaping morphological evolution is incomplete without an appreciation of the distribution of this variation, and the factors generating that distribution. The distribution of morphological variation among phenotypic traits is commonly analyzed in terms of integration, which is defined as the interdependence (i.e., covariance or correlation) of two or more traits (Olson and Miller 1958; Raff 1996; von Dassow and Munro 1999; Gilbert and Bolker 2001; Wagner et al 2007; Willmore et al 2007; Goswami and Polly 2010).

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