Breaking evolutionary and pleiotropic constraints in mammals: On sloths, manatees and homeotic mutations

Varela-Lasheras, Irma; Bakker, Alexander J.; Mije, Steven van der; Metz, J.A.J.; Alphen, Joris van; Galis, Frietson

doi:10.1186/2041-9139-2-11

Cited by 118 publications

(158 citation statements)

References 114 publications

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“…All achieve this by homeotic frameshifts of the thoracic expression pattern (the development of ribs, etc.) relative to the underlying somites [191]. Such shifts in other mammals may be linked to highly deleterious, pleiotropic side effects, not least problems with the innervation, musculature and blood supply of the forelimbs and elevated rates of juvenile cancer [192].…”

Section: Intrinsic Developmental Constraintsmentioning

confidence: 99%

What limits the morphological disparity of clades?

et al. 2015

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The morphological disparity of species within major clades shows a variety of trajectory patterns through evolutionary time. However, there is a significant tendency for groups to reach their maximum disparity relatively early in their histories, even while their species richness or diversity is comparatively low. This pattern of early high-disparity suggests that there are internal constraints (e.g. developmental pleiotropy) or external restrictions (e.g. ecological competition) upon the variety of morphologies that can subsequently evolve. It has also been demonstrated that the rate of evolution of new character states decreases in most clades through time (character saturation), as does the rate of origination of novel bodyplans and higher taxa. Here, we tested whether there was a simple relationship between the level or rate of character state exhaustion and the shape of a clade's disparity profile: specifically, its centre of gravity (CG). In a sample of 93 extinct major clades, most showed some degree of exhaustion, but all continued to evolve new states up until their extinction. Projection of states/steps curves suggested that clades realized an average of 60% of their inferred maximum numbers of states. Despite a weak but significant correlation between overall levels of homoplasy and the CG of clade disparity profiles, there were no significant relationships between any of our indices of exhaustion curve shape and the clade disparity CG. Clades showing early high-disparity were no more likely to have early character saturation than those with maximum disparity late in their evolution.

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Section: Intrinsic Developmental Constraintsmentioning

confidence: 99%

What limits the morphological disparity of clades?

et al. 2015

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“…The left and right halves of transitional vertebrae were often transformed to a different extent, leading to strong left-right asymmetry ( Fig. 2 K and L) (5,9). Partially sacralized lumbar vertebrae were considered to be transitional lumbosacral vertebrae when at least on one side the transverse process was enlarged to such an extent that it was fused with, or touching, the adjacent sacral vertebra or the ilium (Fig.…”

Section: Methodsmentioning

confidence: 99%

“…5 for a more detailed discussion). We expect biomechanical problems to be important because initial mutations for homeotic transformations of vertebrae usually lead to incomplete and often asymmetric transitional vertebrae (9). In the case of lumbosacral transitional vertebrae, this implies incomplete ( Fig.…”

mentioning

confidence: 99%

Fast running restricts evolutionary change of the vertebral column in mammals

Galis

Carrier

Alphen

et al. 2014

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

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The mammalian vertebral column is highly variable, reflecting adaptations to a wide range of lifestyles, from burrowing in moles to flying in bats. However, in many taxa, the number of trunk vertebrae is surprisingly constant. We argue that this constancy results from strong selection against initial changes of these numbers in fast running and agile mammals, whereas such selection is weak in slower-running, sturdier mammals. The rationale is that changes of the number of trunk vertebrae require homeotic transformations from trunk into sacral vertebrae, or vice versa, and mutations toward such transformations generally produce transitional lumbosacral vertebrae that are incompletely fused to the sacrum. We hypothesize that such incomplete homeotic transformations impair flexibility of the lumbosacral joint and thereby threaten survival in species that depend on axial mobility for speed and agility. Such transformations will only marginally affect performance in slow, sturdy species, so that sufficient individuals with transitional vertebrae survive to allow eventual evolutionary changes of trunk vertebral numbers. We present data on fast and slow carnivores and artiodactyls and on slow afrotherians and monotremes that strongly support this hypothesis. The conclusion is that the selective constraints on the count of trunk vertebrae stem from a combination of developmental and biomechanical constraints.M any mammalian taxa show a remarkable conservation of the presacral vertebral count (the sum of cervical, thoracic, and lumbar vertebrae; Fig. 1). For instance, carnivores almost invariably have 27 vertebrae, and artiodactyls have 26 presacral vertebrae. However, in some taxa, in particular afrotherians, there is considerable interspecific variation (1, 2). Narita and Kuratani (1) proposed that the presacral vertebral count is conserved because of developmental constraints, as is also the case for the cervical vertebral count (3, 4). We propose that developmental constraints are indeed involved and that they are interacting with biomechanical problems resulting from homeotic transformations. Homeotic transformations are necessary for changes of the presacral vertebral count (5), although it is often incorrectly thought that these changes can be solely the result of increases or decreases in the number of vertebrae of a certain region. This assumption is not true, except for vertebrae in the tail region, which is the part of the vertebral column formed last. Homeotic transformations are necessarily involved, because of the sequential head-to-tail generation of the embryonal segments from which the vertebrae develop (somites) and the patterning of these segments under the influence of head-to-tail signaling gradients (6-8). This process implies that if there is an increase in the presacral count, for instance from 26 to 27, this is caused by a homeotic transformation of the 27th vertebra from a sacral into a lumbar one, regardless of whether the total count of vertebrae changes or not (see ref. 5 for a more detailed ...

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“…In other tetrapods, the number of cervical vertebrae varies considerably, and in mammals the number of vertebrae in more caudal vertebral regions is variable as well (Leboucq 1896Schultz 1961Starck 1979;Narita & Kuratani 2005). Only manatees (Trichechus, Sirenia) and sloths (Bradypus and Choloepus, Xenarthra) have an exceptional number of cervical vertebrae (Bateson 1894;Starck 1979;Varela-Lasheras et al 2011). Despite the extreme evolutionary conservation of the number of cervical vertebrae, intraspecific variation is not uncommon in mammals.…”

Section: Introductionmentioning

confidence: 99%

“…We have shown that changes of this number are selected against due to a coupling with major congenital abnormalities (pleiotropic effects, (Galis 1999, Galis et al 2006, Varela-Lasheras et al 2011, ten Broek et al 2012). Here we show that the incidence of abnormal cervical vertebral numbers in Late Pleistocene mammoths from the North Sea is high (33.3%) and approximately 10 times higher than that of extant elephants (3.6%).…”

Section: Introductionmentioning

confidence: 99%

Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths

Reumer

Broek

Galis

2014

Preprint

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The number of cervical vertebrae in mammals is highly conserved at seven. We have shown that changes of this number are selected against due to a coupling with major congenital abnormalities (pleiotropic effects, (Galis 1999, Galis et al. 2006, Varela-Lasheras et al. 2011, ten Broek et al. 2012). Here we show that the incidence of abnormal cervical vertebral numbers in Late Pleistocene mammoths from the North Sea is high (33.3%) and approximately 10 times higher than that of extant elephants (3.6%). Abnormal numbers were due to the presence of large cervical ribs on the seventh vertebra, which we deduced from the presence of rib articulation facets on sixth (posterior side) and seventh (anterior side) cervical vertebrae. The incidence of abnormal cervical vertebral numbers in mammoths appears to be much higher than in other mammalian species, apart from exceptional sloths, manatees and dugongs (Varela-Lasheras, Bakker et al. 2011) and indicates a vulnerable condition. We argue that the increased incidence of cervical ribs in mammoths is probably caused by inbreeding and adverse conditions that impact early pregnancies in declining populations close to extinction in the Late Pleistocene.PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.263v1 | CC-BY 4.0

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Breaking evolutionary and pleiotropic constraints in mammals: On sloths, manatees and homeotic mutations

Cited by 118 publications

References 114 publications

What limits the morphological disparity of clades?

What limits the morphological disparity of clades?

Fast running restricts evolutionary change of the vertebral column in mammals

Extraordinary incidence of cervical ribs indicates vulnerable condition in Late Pleistocene mammoths

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