Diversification of the Ruminant Skull Along an Evolutionary Line of Least Resistance

Rhoda, Daniel; Haber, Annat; Angielczyk, Kenneth D.

doi:10.1101/2022.09.13.507810

Cited by 7 publications

(14 citation statements)

References 116 publications

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“…Therefore, a finding of significant allometry in a PGLS test alongside a significant phylogenetic signal of cranial size might indicate that size variation is influenced by a developmental constraint on shape that is consistent regardless of relatedness. This would agree with previous suggestions that allometry explains the majority of cranial shape diversity in some of these taxa, such as the Bovidae (Bibi & Tyler, 2022; Rhoda et al, 2022) and rodents (Marcy et al, 2020). However, an alternative that could be investigated in the future is that phylogenies comprising speciose taxa with multiple monophyletic groups each spanning much of the total size ranges for the clade, such as bovids and rodents, can limit the impact of including the phylogeny in the model and result in similar statistics to the OLS.…”

Section: Gracilisation Patterns In Mammalian Familiessupporting

confidence: 93%

Section: Gracilisation Patterns In Mammalian Familiessupporting

confidence: 93%

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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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Section: Gracilisation Patterns In Mammalian Familiessupporting

confidence: 93%

Section: Gracilisation Patterns In Mammalian Familiessupporting

confidence: 93%

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

Mitchell,

Sherratt,

Weisbecker

2023

Preprint

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“…However, non-whale aquatic mammals, including piscivorous pinnipeds also show shifts in their nares, rostrums and palates, associated with respiration, sexual dimorphism and feeding behaviour [72]. Herbivores show the fastest rates of evolution in anterior face and zygomatic region, reflecting elongation of the face and modification of the premaxilla for either ever-growing incisors or entire loss of these teeth [146,149–152], as well as presence of a complete postorbital bar in many herbivores, such as equids, some artiodactyls, and primates [116,135,149]. By contrast, carnivores show the fastest evolution for the midface and vault, with the latter potentially reflecting increased attachment area for the temporalis muscle [73,102,137,138,153–155].…”

Section: Discussionmentioning

confidence: 99%

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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“…Evolutionary theory predicts that over short, microevolutionary, timescales phenotypic evolution will tend to follow evolutionary lines of genetic least resistance [6, 7]. Over longer timescales, the evolutionary line of least resistance is analogous to the major axis of phenotypic variation [8, 9].…”

Section: Mainmentioning

confidence: 99%

Innovation and elaboration on the avian tree of life

Guillerme

Cooper

Beckerman

et al. 2022

Preprint

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Patterns of biological diversity across the tree of life are the result of millions of years of evolutionary history and are shaped by natural selection. A long-standing proposal is that most morphological diversity among species arises along "an evolutionary line of least resistance", where new phenotypes arise primarily by elaboration - evolution along this line of least resistance. At macro and mega-evolutionary scales, however, we frequently observe major shifts in phenotypes among lineages. The presence of distinct morphological forms suggests instead that diversity can arise via innovation - where species evolve away from the line of least resistance. Here we apply new multi-trait methods to evaluate the magnitude and distribution of elaboration and innovation in the evolution of bird beaks. Our analyses show that elaboration is a common feature at all scales, consistent with theory. We also find that innovation is a common and major contributor to avian morphological diversity among clades. Furthermore, we show that these patterns of innovation are replicated hierarchically throughout avian evolutionary history. These results suggest that both elaboration and innovation are ubiquitous from macro- to mega-evolutionary scales, and that macroevolutionary axes of multivariate evolution are frequently reoriented throughout the history of life, opening up new avenues for evolution to explore.

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Diversification of the Ruminant Skull Along an Evolutionary Line of Least Resistance

Cited by 7 publications

References 116 publications

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

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

Developmental origin underlies evolutionary rate variation across the placental skull

Innovation and elaboration on the avian tree of life

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