An official website of the United States government
Synopsis Mammals exhibit a diverse range of limb morphologies that are associated with different locomotor ecologies and structural mechanics. Much remains to be investigated, however, about the combined effects of locomotor modes and scaling on the external shape and structural properties of limb bones. Here, we used squirrels (Sciuridae) as a model clade to examine the effects of locomotor mode and scaling on the external shape and structure of the two major limb bones, the humerus and femur. We quantified humeral and femoral morphologies using 3D geometric morphometrics and bone structure analyses on a sample of 76 squirrel species across their four major ecotypes. We then used phylogenetic generalized linear models to test how locomotor ecology, size, and their interaction influenced morphological traits. We found that size and locomotor mode exhibit different relationships with the external shape and structure of the limb bones, and that these relationships differ between the humerus and femur. External shapes of the humerus and, to a lesser extent, the femur are best explained by locomotor ecology rather than by size, whereas structures of both bones are best explained by interactions between locomotor ecology and scaling. Interestingly, the statistical relationships between limb morphologies and ecotype were lost when accounting for phylogenetic relationships among species under Brownian motion. That assuming Brownian motion confounded these relationships is not surprising considering squirrel ecotypes are phylogenetically clustered; our results suggest that humeral and femoral variation partitioned early between clades and their ecomorphologies were maintained to the present. Overall, our results show how mechanical constraints, locomotor ecology, and evolutionary history may enact different pressures on the shape and structure of limb bones in mammals.
more »
« less
Scaling patterns of body plans differ among squirrel ecotypes
Body size is often hypothesized to facilitate or constrain morphological diversity in the cranial, appendicular, and axial skeletons. However, how overall body shape scales with body size ( i.e. , body shape allometry) and whether these scaling patterns differ between ecological groups remains poorly investigated. Here, we test whether and how the relationships between body shape, body size, and limb lengths differ among species with different locomotor specializations, and describe the underlying morphological components that contribute to body shape evolution among squirrel (Sciuridae) ecotypes. We quantified the body size and shape of 87 squirrel species from osteological specimens held at museum collections. Using phylogenetic comparative methods, we first found that body shape and its underlying morphological components scale allometrically with body size, but these allometric patterns differ among squirrel ecotypes: chipmunks and gliding squirrels exhibited more elongate bodies with increasing body sizes whereas ground squirrels exhibited more robust bodies with increasing body size. Second, we found that only ground squirrels exhibit a relationship between forelimb length and body shape, where more elongate species exhibit relatively shorter forelimbs. Third, we found that the relative length of the ribs and elongation or shortening of the thoracic region contributes the most to body shape evolution across squirrels. Overall, our work contributes to the growing understanding of mammalian body shape evolution and how it is influenced by body size and locomotor ecology, in this case from robust subterranean to gracile gliding squirrels.
more »
« less
- PAR ID:
- 10398049
- Date Published:
- Journal Name:
- PeerJ
- Volume:
- 11
- ISSN:
- 2167-8359
- Page Range / eLocation ID:
- e14800
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Esselstyn, Jacob (Ed.)Abstract Although convergence is often recognized as a ubiquitous feature across the Tree of Life, whether the underlying traits also exhibit similar evolutionary pathways towards convergent forms puzzles biologists. In carnivoran mammals, “elongate,” “slender,” and “long” are often used to describe and even to categorize mustelids (martens, polecats, and weasels), herpestids (mongooses), viverrids (civets and genets), and other carnivorans together. But just how similar these carnivorans are and whether there is convergence in the morphological component that contribute to elongation has never been assessed. Here, I found that these qualitatively described elongate carnivorans exhibited incomplete convergence towards elongate bodies compared to other terrestrial carnivorans. In contrast, the morphological components underlying body shape variation do not exhibit convergence despite evidence that these components are more elongate in elongate carnivorans compared to nonelongate carnivorans. Furthermore, these components also exhibited shorter but different phylogenetic half-lives towards more elongate adaptive peaks, indicating that different selective pressures can create multiple pathways to elongation. Incorporating the fossil record will facilitate further investigation of whether body elongation evolved adaptively or if it is simply a retained ancestral trait.[Axial skeleton; body elongation; convergent evolution; macroevolution; phylogenetic comparative methods; thoracolumbar vertebrae.]more » « less
-
Abstract The early diversification of tetrapods into terrestrial environments involved adaptations of their locomotor apparatus that allowed for weight support and propulsion on heterogeneous surfaces. Many lineages subsequently returned to the water, while others conquered the aerial environment, further diversifying under the physical constraints of locomoting through continuous fluid media. While many studies have explored the relationship between locomotion in continuous fluids and body mass, none have focused on how continuous fluid media have impacted the macroevolutionary patterns of limb shape diversity.We investigated whether mammals that left terrestrial environments to use air and water as their main locomotor environment experienced constraints on the morphological evolution of their forelimb, assessing their degree of morphological disparity and convergence. We gathered a comprehensive sample of more than 800 species that cover the extant family‐level diversity of mammals, using linear measurements of the forelimb skeleton to determine its shape and size.Among mammals, fully aquatic groups have the most disparate forelimb shapes, possibly due to the many different functional roles performed by flippers or the relaxation of constraints on within‐flipper bone proportions. Air‐based locomotion, in contrast, is linked to restricted forelimb shape diversity. Bats and gliding mammals exhibit similar morphological patterns that have resulted in partial phenotypic convergence, mostly involving the elongation of the proximal forelimb segments.Thus, whereas aquatic locomotion drives forelimb shape diversification, aerial locomotion constrains forelimb diversity. These results demonstrate that locomotion in continuous fluid media can either facilitate or limit morphological diversity and more broadly that locomotor environments have fostered the morphological and functional evolution of mammalian forelimbs. Read the freePlain Language Summaryfor this article on the Journal blog.more » « less
-
Abstract Members of an ecological guild may be anticipated to show morphological convergence, as similar functional demands exert similar selective pressures on phenotypes. Nature is rife with examples, however, where such taxa instead exhibit ‘incomplete’ convergence or even divergence. Incorporating factors such as character displacement by other guild members or variation in ecological specialization itself may therefore be necessary to gain a more complete understanding of what constrains or promotes diversity. Cleaning, a behavior in which species remove and consume ectoparasites from “clientele,” has been shown to exhibit variation in specialization and has evolved in a variety of marine habitats around the globe. To determine the extent to which specialization in this tropic strategy has affected phenotypic evolution, we examined the evolution of cleaning behavior in five marine fish families: Labridae, Gobiidae, Pomacanthidae, Pomacentridae, and Embiotocidae. We used a comparative framework to determine patterns of convergence and divergence in body shape and size across non-cleaning and cleaning members within these five clades. Highly specialized obligate cleaning, found in the Indo-Pacific and the Caribbean, evolved in the Labridae and Gobiidae at strikingly similar times. In these two regions, obligate cleaning evolves early, shows convergence on an elongate body shape, and is restricted to species of small body size. Facultative cleaning, shown either throughout ontogeny or predominately in the juvenile phase, exhibits a much more varied phenotype, especially in geographic regions where obligate cleaning occurs. Collectively, our results are consistent with varying extents of an ecological specialization constraining or spurring morphological evolution in recurrent ways across regions.more » « less
-
null (Ed.)Social insects exhibit highly variable body plans at multiple scales: within colonies, between conspecific colonies, and across different species. The interspecific variation in the existence and prevalence of morphologically discrete worker subcastes in social insects raises questions about the ontogeny and functional importance of alternative worker body plans. Here, we examine the allometry of four Formica species. Formica are among the most common ants in the northern hemisphere temperate zone, and species vary greatly in the degree of worker size variation. However, no Formica species exhibit obvious worker subcastes. By carefully measuring head width, head height, scape length, thorax length, hind femur length, and hind tibia length in 180 individuals, we confirm that Formica workers exhibit continuous linear scaling, meaning that they lack discrete morphological subcastes. Most measurements scale allometrically. Different colonies of the same species are generally consistent in the slope of these relationships, and we detect unexpected similarities in scaling relationships among the four Formica species as well. Some scaling relationships, including a proportionally shorter scape and larger head in large-bodied workers, were also previously found in fire ants. Identifying worker size and shape distributions among different species is a vital step in understanding the selection pressures shaping division of labor in insect societies.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.7717/peerj.14800
