Weak genetic signal for phenotypic integration implicates developmental processes as major regulators of trait covariation

Conith, Andrew J.; Hope, Sylvie A; Chhouk, Brian; Albertson, R. Craig

doi:10.1111/mec.15748

Cited by 11 publications

(14 citation statements)

References 76 publications

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“…Traditionally, much of the study of evolutionary innovation has focused on extrinsic drivers, such as ecological change or environmental stimuli, which have frequently been viewed as the principal triggers for evolutionary novelty ( 6 – 9 ). Recently, focus has shifted toward the effects of intrinsic (e.g., developmental) processes that may structure patterns of trait diversification ( 10 – 12 ). Among these processes, integration and modularity have emerged as important sources of insight as a growing consensus has found that patterns of trait covariation can constrain and facilitate responses to selection and strongly influence patterns of trait diversification at both contemporary and macroevolutionary timescales ( 13 – 20 ).…”

mentioning

confidence: 99%

Integration drives rapid phenotypic evolution in flatfishes

Evans

Larouche

Watson

et al. 2021

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

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Evolutionary innovations are scattered throughout the tree of life, and have allowed the organisms that possess them to occupy novel adaptive zones. While the impacts of these innovations are well documented, much less is known about how these innovations arise in the first place. Patterns of covariation among traits across macroevolutionary time can offer insights into the generation of innovation. However, to date, there is no consensus on the role that trait covariation plays in this process. The evolution of cranial asymmetry in flatfishes (Pleuronectiformes) from within Carangaria was a rapid evolutionary innovation that preceded the colonization of benthic aquatic habitats by this clade, and resulted in one of the most bizarre body plans observed among extant vertebrates. Here, we use three-dimensional geometric morphometrics and a phylogenetic comparative toolkit to reconstruct the evolution of skull shape in carangarians, and quantify patterns of integration and modularity across the skull. We find that the evolution of asymmetry in flatfishes was a rapid process, resulting in the colonization of novel trait space, that was aided by strong integration that coordinated shape changes across the skull. Our findings suggest that integration plays a major role in the evolution of innovation by synchronizing responses to selective pressures across the organism.

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mentioning

confidence: 99%

Integration drives rapid phenotypic evolution in flatfishes

Evans

Larouche

Watson

et al. 2021

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

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“…However, we provide evidence that African cichlid trophic evolution has generally occurred within the context of a coupled jaw system, a trend that was also recently noted in New World cichlids 14 . We demonstrate further that LOJ-LPJ integration may be due, at least in part, to pleiotropy, a phenomenon that is commonly theorized to determine patterns of covariation and limit evolvability (i.e., 9 , 65 but see 60 ). We postulate that integration between LOJ-LPJ shapes in cichlids is not a constraint, but rather an attribute that promotes rapid shifts in foraging niche 33 , 66 , an ability that should be particularly advantageous in young and/or dynamic environments similar to the East African Rift-Valley.…”

Section: Discussionmentioning

confidence: 53%

“…Another consequence of genetic, developmental, and functional constraints is phenotypic integration, whereby seemingly independent traits vary in unison. While determining the origins of integration has proved difficult (i.e., 60 ), trait integration can facilitate or limit morphological evolution depending on the direction of selection 2 . While phenotypic integration is a population-level metric, integration can have far-reaching effects on macroevolutionary processes such as taxonomic diversification, extinction, and morphological evolution 3 , 7 .…”

Section: Discussionmentioning

confidence: 99%

The cichlid oral and pharyngeal jaws are evolutionarily and genetically coupled

Conith

Albertson

2021

Nat Commun

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Evolutionary constraints may significantly bias phenotypic change, while “breaking” from such constraints can lead to expanded ecological opportunity. Ray-finned fishes have broken functional constraints by developing two jaws (oral-pharyngeal), decoupling prey capture (oral jaw) from processing (pharyngeal jaw). It is hypothesized that the oral and pharyngeal jaws represent independent evolutionary modules and this facilitated diversification in feeding architectures. Here we test this hypothesis in African cichlids. Contrary to our expectation, we find integration between jaws at multiple evolutionary levels. Next, we document integration at the genetic level, and identify a candidate gene, smad7, within a pleiotropic locus for oral and pharyngeal jaw shape that exhibits correlated expression between the two tissues. Collectively, our data show that African cichlid evolutionary success has occurred within the context of a coupled jaw system, an attribute that may be driving adaptive evolution in this iconic group by facilitating rapid shifts between foraging habitats, providing an advantage in a stochastic environment such as the East African Rift-Valley.

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“…Plasticity can impact the strength of integration among modules (Anderson et al, 2014), although how plasticity impacts the pattern of modularity is unclear. Recent studies suggest bone remodelling may operate within an existing modularity pattern (Conith et al, 2020) and that modularity patterns could be determined early in development (Conith et al, 2021). If modularity is determined early in development and becomes canalized, then it may preclude marsupials from obtaining placental‐like modularity patterns via plasticity.…”

Section: Discussionmentioning

confidence: 99%

“…The mechanical loading experienced by marsupial neonates during suckling could produce patterns of modularity in the jaw that reflects the locations of functional inputs, overwriting the initial pattern derived from genetic signals (i.e. Conith et al, 2021) and producing different patterns of modularity between marsupial and placental mammals.…”

Section: Introductionmentioning

confidence: 99%

The influence of divergent reproductive strategies in shaping modularity and morphological evolution in mammalian jaws

Conith

Meagher

Dumont

2021

J of Evolutionary Biology

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Marsupial neonates are born at an earlier developmental stage than placental mammals, but the rapid development of their forelimbs and cranial skeleton allows them to climb to the pouch, begin suckling and complete their development ex utero. The mechanical environment in which marsupial neonates develop is vastly different from that of placental neonates, which exhibit a more protracted development of oral muscles and bones. This difference in reproductive strategy has been theorized to constrain morphological evolution in the oral region of marsupials. Here, we use 3D morphometrics to characterize one of these oral bones, the lower jaw (dentary), and assess modularity (pattern of covariation among traits), morphological disparity and rates of morphological evolution in two clades of carnivorous mammals: the marsupial Dasyuromorphia and placental fissiped Carnivora. We find that dasyuromorph dentaries have fewer modules than carnivorans and exhibit tight covariation between the angular and coronoid processes, the primary attachment sites for jaw‐closing muscles. This pattern of modularity may result from the uniform action of muscles on the developing mandible during suckling. Carnivorans are free from this constraint and exhibit a pattern of modularity that more strongly reflects genetic and developmental signals of trait covariation. Alongside differences in modularity, carnivorans exhibit greater disparity and faster rates of morphological evolution compared with dasyuromorphs. Taken together, this suggests dasyuromorphs have retained a signal of trait covariation that reflects the outsized influence of muscular force during early development, a feature that may have impacted the ability of marsupial carnivores to explore specialized regions of morphospace.

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Weak genetic signal for phenotypic integration implicates developmental processes as major regulators of trait covariation

Cited by 11 publications

References 76 publications

Integration drives rapid phenotypic evolution in flatfishes

Integration drives rapid phenotypic evolution in flatfishes

The cichlid oral and pharyngeal jaws are evolutionarily and genetically coupled

The influence of divergent reproductive strategies in shaping modularity and morphological evolution in mammalian jaws

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