The developmental impacts of natural selection on human pelvic morphology

Abstract

Evolutionary responses to selection for bipedalism and childbirth have shaped the human pelvis, a structure that differs substantially from that in apes. Morphology related to these factors is present by birth, yet the developmental-genetic mechanisms governing pelvic shape remain largely unknown. Here, we pinpoint and characterize a key gestational window when human-specific pelvic morphology becomes recognizable, as the ilium and the entire pelvis acquire traits essential for human walking and birth. We next use functional genomics to molecularly characterize chondrocytes from different pelvic subelements during this window to reveal their developmental-genetic architectures. We then find notable evidence of ancient selection and genetic constraint on regulatory sequences involved in ilium expansion and growth, findings complemented by our phenotypic analyses showing that variation in iliac traits is reduced in humans compared to African apes. Our datasets provide important resources for musculoskeletal biology and begin to elucidate developmental mechanisms that shape human-specific morphology.

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

“…Most of these traits are derived from the ilium, and while they do have biomechanical correlates with locomotor function (see Grabowski & Roseman, 2015), work by Hammond and Almécija (2017) suggests that parts of the ilium may have a greater propensity to independently respond to selection. Recent evo-devo research by Mariel Young et al (2022) has added further evidence to support the uniqueness of evolution in the ilium with respect to other parts of the pelvis in humans. This may be affecting the degree of evolutionary constraint observed between the os coxae and other anatomical regions.…”

“…Researchers who wish to perform such studies that use fossilized remains or limited sample sizes should pay close attention to the cautions of Houle et al (2011) and be explicit about their model assumptions. In addition, while comparisons of groups within a species are possible (Savell, 2020;Young et al, 2022), researchers ought to be diligent to account for population structure, which in studies on humans has proven difficult in cases of imperfect matches between genomic data (for constructing population history) and morphological data (see, e.g., Roseman & Auerbach, 2015;Savell et al, 2016Savell et al, , 2022.…”

“…To test functional trait complexes, researchers would need to combine evolutionary quantitative genetics with developmental models and, ideally, phylogenetic comparative methods. Though this may appear to be a high bar, some studies, such as Young et al (2022), have successfully brought these fields together to ask evolutionary questions about morphology. Such studies are promising glimpses into the potential that these kinds of approaches provide to answer evo-devo questions that emerge from evolutionary quantitative genetic models.…”

“…Estimates of evolvability and integration only provide a framework for the evolutionary potential of traits, but are unable to assess through what processes traits ultimately did evolve and the effect this had on morphological variation. To assess the actual evolutionary processes that led to trait variation, researchers need to use either experimental biology (e.g., Garland & Rose, 2009; Marchini & Rolian, 2018; Roseman et al, 2020; Young et al, 2022) or the comparative method (e.g., Felsenstein, 1985; Harvey & Pagel, 1991; Leroi et al, 1994; Martins, 2000; Martins & Hansen, 1997).…”

“…Thus, quantitative genetics allows for the creation of a more nuanced and robust picture of trait evolution. In addition, this approach highlights regions or subsets of traits that may deserve further evaluation using a combined evolutionary and developmental ("evo-devo") framework, potentially allowing us to narrow down specific mechanisms driving observed change (e.g., Unger et al, 2021;Young et al, 2019Young et al, , 2022.…”