Mammalian forelimb evolution is driven by uneven proximal-to-distal morphological diversity

Abstract

Vertebrate limb morphology often reflects the environment due to variation in locomotor requirements. However, proximal and distal limb segments may evolve differently from one another, reflecting an anatomical gradient of functional specialization that has been suggested to be impacted by the timing of development. Here we explore whether the temporal sequence of bone condensation predicts variation in the capacity of evolution to generate morphological diversity in proximal and distal forelimb segments across more than 600 species of mammals. Distal elements not only exhibit greater shape diversity, but also show stronger within-element integration and, on average, faster evolutionary responses than intermediate and upper limb segments. Results are consistent with the hypothesis that late developing distal bones display greater morphological variation than more proximal limb elements. However, the higher integration observed within the autopod deviates from such developmental predictions, suggesting that functional specialization plays an important role in driving within-element covariation. Proximal and distal limb segments also show different macroevolutionary patterns, albeit not showing a perfect proximo-distal gradient. The high disparity of the mammalian autopod, reported here, is consistent with the higher potential of development to generate variation in more distal limb structures, as well as functional specialization of the distal elements.

Small body size is associated with increased evolutionary lability of wing skeleton proportions in birds

“…This may explain why, although carpometacarpus size is strongly relevant to flight-style across birds, its 3D shape– which might not be evolving under the same constraints– exhibits an even clearer relationship to external wing geometry and flight-style variety 33 , 49 . Our result here is distinct from observations in mammals 57 , in which forelimb evolution exhibits a strong proximo-distal gradient of morphological disparity. This departure in birds from a pattern reflecting the underlying embryogenetic sequence lends further credence to the hypothesis that integration within the avian wing may be under strong mechanical constraint that causes a unique variance structure and evolutionary coalescence around a small range of wing proportions.…”

Predicting body mass in Ruminantia using postcranial measurements

“…At the other extreme, body mass of the ruminants in tribe Antilopini are consistently overpredicted by metacarpus length with an average %PE of roughly −24%, as they have long, gracile extremities and tend to occur in open habitats (Table 4, Figure 3). These patterns provide an interesting platform on which to explore the functional associations between habitat and body mass in ungulates in the future, particularly through a developmental lens where proximal limb segments are more constrained in morphology relative to distal limb elements which may reflect functional variation related to locomotion and habitat (Rothier et al, 2023; Scott, 1985; Young, 2013).…”

“…The use of long bone lengths in fossil ruminant ecology may alternatively be found in reconstructing relationships with habitat, as Scott (1983Scott ( , 1985 suggested that distal limb proportions, in particular, may adapt more quickly to changes in substrate than 4, Figure 3). These patterns provide an interesting platform on which to explore the functional associations between habitat and body mass in ungulates in the future, particularly through a developmental lens where proximal limb segments are more constrained in morphology relative to distal limb elements which may reflect functional variation related to locomotion and habitat (Rothier et al, 2023;Scott, 1985;Young, 2013).…”

“…Then, as more measurement information may increase prediction accuracy, I use stepwise multiple regression models based on individual elements and, in the case of long bones, proximal and distal subsets of measurements as well as suites of measurements related to a single element. Mammalian proximal limb elements exhibit a stronger signal of evolutionary covariation than distal elements (Rothier et al, 2023), which develop later and are more morphologically disparate (Young, 2013), possibly because of the functional demands related to locomotion. I, therefore, expected that proximal measurements would better predict mass in this group.…”

A whale humerus ironically shaped by neutral evolution and morphological integration

“…This puts us back to a discussion about the origins of evolutionary novelty and its relatedness to anatomical (dis)integration (e.g., (Evans et al, 2021;Olson & Miller, 1958;Wagner & Altenberg, 1996;Wagner & Lynch, 2010;Zelditch & Goswami, 2021)). However, the evolutionary patterns observed in the humerus of cetaceans are not universal even across mammals (López-Aguirre et al, 2021;Rothier et al, 2023) and broadening the range of taxa to be examined, especially on the basalmost extinct forms and other deep lineages of aquatic mammals, seems beneficial for understanding the bigger picture which can be quite complex (Goswami et al, 2015;Lungmus & Angielczyk, 2021).…”