The Predictable Complexity of Evolutionary Allometry

Zelditch, Miriam Leah; Swiderski, Donald L.

doi:10.1007/s11692-022-09581-1

Cited by 11 publications

(17 citation statements)

References 82 publications

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“…Body size is often hypothesized to be a line of least evolutionary resistance for morphological evolution ( Marroig & Cheverud, 2005 ; Marroig & Cheverud, 2010 ), and evolutionary changes in body size have a strong influence on an organism’s ecological, physiological, morphological, and functional traits ( Schmidt-Nielsen, 1975 ; LaBarbera, 1989 ; Calder, 2001 ; Pyron & Burbink, 2009 ). Because traits often scale with size, species can adapt to different environments through evolutionary increases or decreases in body size ( Zelditch et al, 2017 ; Zelditch & Swiderski, 2022 ). However, extrinsic and intrinsic factors often constrain bodies towards certain sizes; therefore, in instances when evolutionary change in body size is limited, new adaptations can arise through evolutionary changes in the shape or proportions of traits ( Zelditch et al, 2017 ).…”

Section: Introductionmentioning

confidence: 99%

Scaling patterns of body plans differ among squirrel ecotypes

Linden

Burtner

Rickman

et al. 2023

PeerJ

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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.

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Section: Introductionmentioning

confidence: 99%

Scaling patterns of body plans differ among squirrel ecotypes

Linden

Burtner

Rickman

et al. 2023

PeerJ

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“…Developmental origin is of course not the only factor impacting macroevolutionary trajectories of cranial regions. Size and phylogeny have long been identified as primary factors impacting skull evolution [23,[112][113][114][115][116][117][118], and both are significantly associated with variation in shape for each cranial region studied here. Nonetheless, there is substantial range in their effects across the cranium, as may be expected given the potentially competing functions and pressures experienced by different cranial regions [4,73,105,112,113].…”

Section: Discussionmentioning

confidence: 90%

“…A longstanding hypothesis posits that the face and braincase should show opposing patterns of allometry, with the brain's negative allometry with size buffered by the face's positive allometry, which together result in a near-geometric scaling of the skull overall [112][113][114]123]. The results here support the hypothesis that cranial allometry is dominated by these two regions, and it is noteworthy that the strongest effect is observed in the braincase, though establishing which region drives this pattern of cranial allometry requires explicit analysis [113].…”

Section: Discussionmentioning

confidence: 99%

“…This is perhaps expected, as the allometry of the brain and face in mammals and other big-brained vertebrates has long been a topic of debate [23,112,114,123], driven in large part by a clear negative allometry of brain size and body size that is likely driven by energetic and/or developmental costs of large brains [111,[124][125][126][127]. A longstanding hypothesis posits that the face and braincase should show opposing patterns of allometry, with the brain's negative allometry with size buffered by the face's positive allometry, which together result in a near-geometric scaling of the skull overall [112][113][114]123]. The results here support the hypothesis that cranial allometry is dominated by these two regions, and it is noteworthy that the strongest effect is observed in the braincase, though establishing which region drives this pattern of cranial allometry requires explicit analysis [113].…”

Section: Discussionmentioning

confidence: 99%

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Developmental origin underlies evolutionary rate variation across the placental skull

Goswami

Noirault

Coombs

et al. 2023

Phil. Trans. R. Soc. B

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The placental skull has evolved into myriad forms, from longirostrine whales to globular primates, and with a diverse array of appendages from antlers to tusks. This disparity has recently been studied from the perspective of the whole skull, but the skull is composed of numerous elements that have distinct developmental origins and varied functions. Here, we assess the evolution of the skull's major skeletal elements, decomposed into 17 individual regions. Using a high-dimensional morphometric approach for a dataset of 322 living and extinct eutherians (placental mammals and their stem relatives), we quantify patterns of variation and estimate phylogenetic, allometric and ecological signal across the skull. We further compare rates of evolution across ecological categories and ordinal-level clades and reconstruct rates of evolution along lineages and through time to assess whether developmental origin or function discriminate the evolutionary trajectories of individual cranial elements. Our results demonstrate distinct macroevolutionary patterns across cranial elements that reflect the ecological adaptations of major clades. Elements derived from neural crest show the fastest rates of evolution, but ecological signal is equally pronounced in bones derived from neural crest and paraxial mesoderm, suggesting that developmental origin may influence evolutionary tempo, but not capacity for specialisation. This article is part of the theme issue ‘The mammalian skull: development, structure and function’.

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“…Cranial allometric variation in mammals is often related to changes in the facial dimensions relative to the braincase (Radinsky, 1984a(Radinsky, , 1985Emerson & Bramble, 1993;Zelditch & Swiderski, 2022). CREA captures this by noting that, "Adults of larger species, in a group of closely related mammals, tend to have relatively longer faces and smaller braincases" (Cardini, 2019).…”

Section: How Do We Test For Craniofacial Allometry?mentioning

confidence: 99%

Facing the facts: Adaptive trade-offs along body size ranges determine mammalian craniofacial scaling

Mitchell,

Sherratt,

Weisbecker

2023

Preprint

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The mammalian cranium (skull without lower jaw) is representative of mammalian diversity and is thus of particular interest to mammalian biologists across disciplines. One widely retrieved pattern accompanying mammalian cranial diversification is referred to as “craniofacial evolutionary allometry” (CREA). This posits that “adults of larger species, in a group of closely related mammals, tend to have relatively longer faces and smaller braincases”. However, no process has been officially suggested to explain this pattern, there are many exceptions, and its predictions potentially conflict with well-established biomechanical principles. Understanding the mechanisms behind CREA and causes for deviations from the pattern therefore has tremendous potential to explain allometry and diversification of the mammalian cranium. Here, we propose an amended framework to characterise the CREA pattern more clearly, in that “longer faces” can arise through several kinds of evolutionary change, including elongation of the rostrum, retraction of the jaw muscles, or a more narrow or shallow skull, which all result in a generalised gracilisation of the facial skeleton with increased size. We define a standardised workflow to test for the presence of the pattern, using allometric shape predictions derived from geometric morphometrics analysis, and apply this to 22 mammalian families including marsupials, rabbits, rodents, bats, carnivores, antelope, and whales. Our results show that increasing facial gracility with size is common, but not necessarily as ubiquitous as previously suggested. To address the mechanistic basis for this variation, we then review cranial adaptations for harder biting. These dictate that a more gracile cranium in larger species must represent a sacrifice in the ability to produce or withstand harder bites, relative to size. This leads us to propose that facial gracilisation in larger species is often a product of bite force allometry and phylogenetic niche conservatism, where more closely related species tend to exhibit more similar feeding ecology and biting behaviours and, therefore, absolute (size-independent) bite force requirements. Since larger species can produce the same absolute bite forces as smaller species with less effort, we propose that relaxed bite force demands can permit facial gracility in response to bone optimisation and alternative selection pressures. Thus, mammalian facial scaling represents an adaptive by-product of the shifting importance of selective pressures occurring with increased size. A reverse pattern of facial “shortening” can accordingly also be found, and is retrieved in several cases here, where larger species incorporate novel feeding behaviours involving greater bite forces. We discuss multiple exceptions to a bite force-mediated influence on facial length across mammals which lead us to argue that ecomorphological specialisation of the cranium is likely to be the primary driver of facial scaling patterns, with developmental and/or phylogenetic constraints a secondary factor. A potential for larger species to have a wider range of cranial functions when less constrained by biomechanical demands might also explain why selection for larger sizes seems to be prevalent in some mammalian clades. The interplay between adaptation and constraint across size ranges thus presents an interesting consideration for a mechanistically grounded investigation of mammalian cranial allometry.

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The Predictable Complexity of Evolutionary Allometry

Cited by 11 publications

References 82 publications

Scaling patterns of body plans differ among squirrel ecotypes

Scaling patterns of body plans differ among squirrel ecotypes

Developmental origin underlies evolutionary rate variation across the placental skull

Facing the facts: Adaptive trade-offs along body size ranges determine mammalian craniofacial scaling

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