Polymorphism in developmental timing: intraspecific heterochrony in a Lake Victoria cichlid

Jong, Ilse M.L. de; Colbert, Matthew W.; Witte, Frans; Richardson, Michael K.

doi:10.1111/j.1525-142x.2009.00370.x

Cited by 31 publications

(28 citation statements)

References 41 publications

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“…Alberch and Blanco 1996;Moore 1991). Nonetheless, recent works have demonstrated and underlined that it is imperative to consider patterns of embryonic variability when examining developmental time (Colbert and Rowe 2008;de Jong et al 2009). Consideration of this notion opens a suite of questions in relation to the evolution of developmental sequences.…”

Section: Intraspecific Variation In Ossification Sequencementioning

confidence: 98%

Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia)

et al. 2010

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Data documenting skeletal development in rodents, the most species-rich 'order' of mammals, are at present restricted to a few model species, a shortcoming that hinders exploration of the morphological and ecological diversification of the group. In this study we provide the most comprehensive sampling of rodent ossification sequences to date, with the aim of exploring whether heterochrony is ubiquitous in rodent evolution at the onset of skeletal formation. The onset of ossification in 17 cranial elements and 24 postcranial elements was examined for eight muroid and caviomorph rodent species. New data are provided for two non-model species. For one of these, the African striped mouse, Rhabdomys pumilio, sampling was extended by studying 53 autopodial elements and examining intraspecific variation. The Parsimov method of studying sequence heterochrony was used to explore the role that changes in developmental timing play in early skeletal formation. Few heterochronies were found to diagnose the muroid and caviomorph clades, suggesting conserved patterning in skeletal development. Mechanisms leading to the generation of the wide range of morphological diversity encapsulated within Rodentia may be restricted to later periods in development than those studied in this work. Documentation of skeletogenesis in Rhabdomys indicates that intraspecifc variation in ossification sequence pattern is present, though not extensive. Our study suggests that sequence heterochrony is neither pivotal nor prevalent during early skeletal formation in rodents.

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Section: Intraspecific Variation In Ossification Sequencementioning

confidence: 98%

Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia)

et al. 2010

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“…OSA has normally been used to understand variation and development in extant organisms (32,(56)(57)(58)(59)(60), with only a few previously published studies using this method in extinct taxa (21,61). We followed standard OSA procedure (32) to conduct this analysis.…”

Section: Methodsmentioning

confidence: 99%

Anomalously high variation in postnatal development is ancestral for dinosaurs but lost in birds

Griffin

Nesbitt

2016

Proc. Natl. Acad. Sci. U.S.A.

127

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Compared with all other living reptiles, birds grow extremely fast and possess unusually low levels of intraspecific variation during postnatal development. It is now clear that birds inherited their high rates of growth from their dinosaurian ancestors, but the origin of the avian condition of low variation during development is poorly constrained. The most well-understood growth trajectories of later Mesozoic theropods (e.g., Tyrannosaurus, Allosaurus) show similarly low variation to birds, contrasting with higher variation in extant crocodylians. Here, we show that deep within Dinosauria, among the earliest-diverging dinosaurs, anomalously high intraspecific variation is widespread but then is lost in more derived theropods. This style of development is ancestral for dinosaurs and their closest relatives, and, surprisingly, this level of variation is far higher than in living crocodylians. Among early dinosaurs, this variation is widespread across Pangaea in the Triassic and Early Jurassic, and among early-diverging theropods (ceratosaurs), this variation is maintained for 165 million years to the end of the Cretaceous. Because the Late Triassic environment across Pangaea was volatile and heterogeneous, this variation may have contributed to the rise of dinosaurian dominance through the end of the Triassic Period.I n comparison with other reptiles, avian biology is highly unusual, characterized by "hollow" bones and postcranial skeletal pneumaticity, feathers, a unique forelimb digit formula, endothermy, and rapid growth rates. However, these peculiarities initially arose in nonavian dinosaurs (1-7) in a gradual process occurring over tens of millions of years (8,9). In addition to their extremely rapid rates of growth, avian ontogeny possesses a characteristically low level of morphological variation within a species relative to that of other reptiles. The majority of individuals in a given avian species undergoes the same morphological changes during ontogeny in the same order at similar body sizes (10, 11), whereas their closest living relatives, crocodylians, possess higher variation (10,(12)(13)(14). How and when this feature of avian biology evolved is poorly constrained.This avian style of development must have evolved after its most recent common ancestor with crocodylians but before the origin of Aves. Most studies of the ontogeny of more-derived theropods (15-17) suggest that the low levels of variation that characterize avian ontogeny were present in close nonavian relatives as well. Closer to the origin of Dinosauria, morphological variation within species is widespread (18-26), but whether this variation is the result of taxonomic diversity, ontogeny, sexual dimorphism, or simple individual variation is not clear (22,23,27). Furthermore, close dinosaurian relatives or "dinosaur precursors" (e.g., Silesaurus, Asilisaurus) possess high intraspecific variation in growth sequences [i.e., sequence polymorphism (28)], suggesting that this condition could be ancestral for Dinosauria (21).In contrast to ...

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“…For example, de Jong [15] showed, using 82 developmental characters in 261 embryos of the cichlid, Haplochromis piceatus, that embryos could follow one of 26 880 different developmental sequences [15]. This magnitude (and complexity) of intraspecific variation is astounding and demonstrates that intraspecific developmental event timing is far from invariant.…”

Section: Introductionmentioning

confidence: 99%

“…For intraspecific variation in developmental event timing to be the raw material from which heterochronies arise requires that it should have both a genetic basis and be heritable. Heritability of developmental event timing would point to intraspecific variation, of which there is increasing evidence [10,15], as an origin of the macroevolutionary pattern of heterochrony.…”

Section: Introductionmentioning

confidence: 99%

Parent–offspring similarity in the timing of developmental events: an origin of heterochrony?

2013

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Understanding the link between ontogeny (development) and phylogeny (evolution) remains a key aim of biology. Heterochrony, the altered timing of developmental events between ancestors and descendants, could be such a link although the processes responsible for producing heterochrony, widely viewed as an interspecific phenomenon, are still unclear. However, intraspecific variation in developmental event timing, if heritable, could provide the raw material from which heterochronies originate. To date, however, heritable developmental event timing has not been demonstrated, although recent work did suggest a genetic basis for intraspecific differences in event timing in the embryonic development of the pond snail, Radix balthica. Consequently, here we used high-resolution (temporal and spatial) imaging of the entire embryonic development of R. balthica to perform a parent -offspring comparison of the timing of twelve, physiological and morphological developmental events. Between-parent differences in the timing of all events were good predictors of such timing differences between their offspring, and heritability was demonstrated for two of these events (foot attachment and crawling). Such heritable intraspecific variation in developmental event timing could be the raw material for speciation events, providing a fundamental link between ontogeny and phylogeny, via heterochrony.

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Polymorphism in developmental timing: intraspecific heterochrony in a Lake Victoria cichlid

Cited by 31 publications

References 41 publications

Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia)

Skeletogenesis and sequence heterochrony in rodent evolution, with particular emphasis on the African striped mouse, Rhabdomys pumilio (Mammalia)

Anomalously high variation in postnatal development is ancestral for dinosaurs but lost in birds

Parent–offspring similarity in the timing of developmental events: an origin of heterochrony?

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