Morphology, evolution, and the whole organism imperative: Why evolutionary questions need multi-trait evolutionary quantitative genetics.

Since Washburn's New Physical Anthropology, researchers have sought to understand the complexities of morphological evolution among anatomical regions in human and non-human primates. Researchers continue, however, to preferentially use comparative and functional approaches to examine complex traits, but these methods cannot address questions about evolutionary process and often conflate function with fitness. Moreover, researchers also tend to examine anatomical elements in isolation, which implicitly assumes independent evolution among different body regions. In this paper, we argue that questions asked in primate evolution are best examined using multiple anatomical regions subjected to model-bound methods built from an understanding of evolutionary quantitative genetics. A nascent but expanding number of studies over the last two decades use this approach, examining morphological integration, evolvability, and selection modeling. To help readers learn how to use these methods, we review fundamentals of evolutionary processes within a quantitative genetic framework, explore the importance of neutral evolutionary theory, and explain the basics of evolutionary quantitative genetics, namely the calculation of evolutionary potential for multiple traits in response to selection. Leveraging these methods, we demonstrate their use to understand non-independence in possible evolutionary responses across the limbs, limb girdles, and basicranium of humans. Our results show that model-bound quantitative genetic methods can reveal unexpected genetic covariances among traits that create a novel but measurable understanding of evolutionary complexity among multiple traits. We advocate for evolutionary quantitative genetic methods to be a standard whenever appropriate to keep studies of primate morphological evolution relevant for the next seventy years and beyond.

Morphological integration and evolutionary potential of the primate shoulder: Variation among taxa and implications for genetic covariances with the basicranium, pelvis, and arm.

Within the primate order, the morphology of the shoulder girdle is immensely variable and has been shown to reflect the functional demands of the upper limb. The observed morphological variation among extant primate taxa consequently has been hypothesized to be driven by selection for different functional demands. Evolutionary analyses of the shoulder girdle often assess this anatomical region, and its traits, individually, therefore implicitly assuming independent evolution of the shoulder girdle. However, the primate shoulder girdle has developmental and functional covariances with the basicranium and pelvic girdle that have been shown to potentially influence its evolution. It is unknown whether these relationships are similar or even present across primate taxa, and how they may affect morphological variation among primates. This study evaluates the strength of covariance and evolutionary potential across four anatomical regions: shoulder girdle, basicranium, pelvis, and distal humerus. Measures of morphological integration and evolutionary potential (conditioned covariance and evolutionary flexibility) are assessed across eight anthropoid primate taxa. Results demonstrate a consistent pattern of morphological constraint within paired anatomical regions across primates. Differences in evolutionary flexibility are observed among primate genera, with humans having the highest evolutionary potential overall. This pattern does not follow functional differences, but rather a separation between monkeys and apes. Therefore, evolutionary hypotheses of primate shoulder girdle morphological variation that evaluate functional demands alone may not account for the effect of these relationships. Collectively, our findings suggest differences in genetic covariance among anatomical regions may have contributed to the observable morphological variation among taxa.