Evolvability and constraint in the primate basicranium, shoulder, and hip and the importance of multi-trait evolution

Abstract

The scapula shares developmental and functional relationships with traits of the basicranium, vertebral column, humerus, and clavicle. As a limb girdle, it also shares analogous characteristics with the pelvis. Despite these relationships, studies of primate shoulder evolution often focus on traits of the scapula in isolation. Such analyses may lead to spurious conclusions, as they implicitly model the scapula as evolving independent of other anatomical regions. Traits of the shoulder girdle share genetic covariances with each other, as well as potential covariances with dimensions of other skeletal elements. To create accurate models of shoulder evolution, it is imperative to account for the constraints imposed by these sources of covariance. Here, we use evolutionary quantitative methods to test a model in which shoulder morphological evolution is influenced by its developmental and functional covariances with the basicranium in the Colobus genus. This evolutionary relationship is also assessed with morphology of the pelvis to provide context to the evolutionary covariance among traits of the basicranium and shoulder girdle. Our results indicate potential evolutionary implications arising from covariances among the basicranium, shoulder, and pelvis. We further propose that the shoulder and basicranium may be examples of developmental, functional, and genetic covariances among traits that manifest an evolutionary suite of mutually constrained morphologies. We demonstrate novel evolutionary relationships among the shoulder girdle and basicranium that affect not only models of primate shoulder evolution but have broader implications for modeling trait evolution across the skeleton.

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

“…This result aligns with known developmental and functional relationships among these anatomical regions. Overall, Agosto and Auerbach (2021) demonstrated that the evolution of the primate shoulder is more complex than previously perceived, uncovering evolutionary covariance with anatomical regions once assumed to be independent of the shoulder (i.e., the basicranium). These relationships, however, are not evident when evaluating the scapula or its traits alone.…”

“…We expect that there will be evidence that, especially for the basicranium, shoulder, and pelvis, relationships with each other will lead to constraints in the evolutionary potential of the traits within each anatomical region, following the results of Agosto and Auerbach (2021).…”

“…Additional analyses by Agosto and Auerbach (2021), which include traits of the proximal humerus, also demonstrate greater potential evolutionary independence of these traits from the basicranium and pelvis compared with the scapula. This result aligns with known developmental and functional relationships among these anatomical regions.…”

“…Furthermore, the results suggest the basicranium imposes evolutionary constraint on both the shoulder and pelvic girdles but is not equally constrained by either the shoulder girdle or pelvic girdle. Additional analyses by Agosto and Auerbach (2021), which include traits of the proximal humerus, also demonstrate greater potential evolutionary independence of these traits from the basicranium and pelvis compared with the scapula. This result aligns with known developmental and functional relationships among these anatomical regions.…”

Evolvability in the fossil record

“…This assumes that the estimated P or G from the extant population is similar enough to G in the ancestral, extinct population. Based on similarities between closely related extant species, a wide array of work (both neontological and paleontological) has assumed that P (or G ) from an extant population is representative of the ancestral G , which has allowed researchers to make evolutionary inferences from phenotypic data across macroevolutionary timescales in ways that would otherwise be impossible (Ackermann and Cheverud 2004; de Oliveira et al 2009; Rolian 2009; Marroig and Cheverud 2010; Young et al 2010; Grabowski et al 2011; Grabowski 2013; Baab 2018; Villamil 2018; Savell 2020; Agosto and Auerbach 2021).…”