Neural crest cells as a source of microevolutionary variation

Brandon, A. Allyson; Almeida, Daniela; Powder, Kara E.

doi:10.1016/j.semcdb.2022.06.001

Cited by 12 publications

(16 citation statements)

References 154 publications

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“…What factors are most important for morphological diversification? Many deep-time studies focus on environment and ecology as the key forces governing selection [3,7,12,[101][102][103], but developmental patterning and genetic interactions of traits generate the variation upon which natural selection can act and thus are also critical for shaping morphological evolution [14,17,45,57,59]. Discerning the relative importance of extrinsic and intrinsic factors is complicated, as hypotheses of developmental and functional patterning often overlap [25,66].…”

Section: Discussionmentioning

confidence: 99%

“…However, these areas of conservation or convergence are not evenly spread across the skull, nor are areas of divergence (figure 3; electronic supplementary material, figure S1), which may reflect different functions of skull regions or their divergent developmental origins, or both. The pluripotency of neural crest cells has often been suggested to drive morphological novelty, as in the formation of the vertebrate head and jaw [51,56], and more recently has been invoked as a driver of morphological variation in domesticated species [58][59][60] and sexually selected traits [57].…”

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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Section: Discussionmentioning

confidence: 99%

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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“…Similarly, differential expression levels of pax3a , mediating xanthophore specification from the NC (Minchin and Hughes, 2008), have been implicated in continuous variation in colour patterns in L. fuelleborni and Tropheops ‘red cheek’ (Lake Malawi) (Albertson et al, 2014). Despite the compelling evidence suggesting the role of NC in the morphological diversity of cichlids, the innate patterns of NCC migration, as well as more general features of the NC development, remain to be explored in the cichlid system (Brandon et al, 2022).…”

Section: Discussionmentioning

confidence: 99%

“…The copyright holder for this preprint this version posted September 17, 2022. ; https://doi.org/10.1101/2022.09.16.508246 doi: bioRxiv preprint patterns of NCC migration, as well as more general features of the NC development, remain to be explored in the cichlid system (Brandon et al, 2022).…”

Section: The Species-specific Phenotypes Of Nc-derived Traits Are Det...mentioning

confidence: 99%

Morphological and temporal variation in early embryogenesis contributes to species divergence in Malawi cichlid fishes

Marconi

Yang

McKay

et al. 2022

Preprint

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The cichlid fishes comprise the largest extant vertebrate family and are the quintessential example of rapid "explosive" adaptive radiations and phenotypic diversification. Despite low genetic divergence, East African cichlids harbour a spectacular intra- and interspecific morphological diversity, including the hyper-variable, neural crest (NC)-derived traits such as colouration and craniofacial skeleton. Although the genetic and developmental basis of these phenotypes has been investigated, understanding of when, and specifically how early, in ontogeny species-specific differences emerge, remains limited. Since adult traits often originate during embryonic development, the processes of embryogenesis could serve as a potential source of species-specific variation. Consequently, we compared the features of embryogenesis between three Malawi cichlid species - Astatotilapia calliptera, Tropheops sp. 'mauve' and Rhamphochromis sp. 'chilingali' - representing a wide spectrum of variation in pigmentation and craniofacial morphologies. Our results showed fundamental differences in multiple aspects of embryogenesis that could underlie interspecific divergence in adult adaptive traits. Firstly, we identified variation in the somite number and signatures of temporal variation, or heterochrony, in the rates of somite formation. The heterochrony was also evident within and between species throughout ontogeny, up to the juvenile stages. Finally, the identified interspecific differences in the development of pigmentation and craniofacial cartilages, present at the earliest stages of their overt formation, provide compelling evidence that the species-specific trajectories begin divergence during early embryogenesis, potentially during somitogenesis and NC development. Altogether, our results expand our understanding of fundamental cichlid biology and provide new insights into the developmental origins of vertebrate morphological diversity.

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“…Briefly, we argue this is simply due to the high proportion of reproductively relevant vertebrate features which derive from the neural crest. These provide regular targets for natural and sexual selection, and are common catalysts of taxonomic differentiation and speciation; whether via male adaptations for fighting and signalling [ 53 ], or a range of other pathways [ 79 ]. As such, any significant selective regime change (under domestication, or other ecological circumstances) should predictably, but only coincidentally, often affect traits and features derived from these vertebrate cells, whose contributions continue to be elaborated by science [ 11 ].…”

Section: An Alternative View Of Ncc Changesmentioning

confidence: 99%

Shared reproductive disruption, not neural crest or tameness, explains the domestication syndrome

Gleeson

Wilson

2023

Proc. R. Soc. B.

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Altered neural crest cell (NCC) behaviour is an increasingly cited explanation for the domestication syndrome in animals. However, recent authors have questioned this explanation, while others cast doubt on whether domestication syndrome even exists. Here, we review published literature concerning this syndrome and the NCC hypothesis, together with recent critiques of both. We synthesize these contributions and propose a novel interpretation, arguing shared trait changes under ancient domestication resulted primarily from shared disruption of wild reproductive regimes. We detail four primary selective pathways for ‘reproductive disruption' under domestication and contrast these succinct and demonstrable mechanisms with cryptic genetic associations posited by the NCC hypothesis. In support of our perspective, we illustrate numerous important ways in which NCCs contribute to vertebrate reproductive phenotypes, and argue it is not surprising that features derived from these cells would be coincidentally altered under major selective regime changes, as occur in domestication. We then illustrate several pertinent examples of Darwin's ‘unconscious selection' in action, and compare applied selection and phenotypic responses in each case. Lastly, we explore the ramifications of reproductive disruption for wider evolutionary discourse, including links to wild ‘self-domestication' and ‘island effect’, and discuss outstanding questions.

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Neural crest cells as a source of microevolutionary variation

Cited by 12 publications

References 154 publications

Developmental origin underlies evolutionary rate variation across the placental skull

Developmental origin underlies evolutionary rate variation across the placental skull

Morphological and temporal variation in early embryogenesis contributes to species divergence in Malawi cichlid fishes

Shared reproductive disruption, not neural crest or tameness, explains the domestication syndrome

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