Integration drives rapid phenotypic evolution in flatfishes

Abstract

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.

Quantifying asymmetry in non-symmetrical morphologies, with an example from Cetacea

“…The eyes of most flatfishes sit on the same side of the head; a development that happens during the larval stage where one eye of a symmetrical lava migrates to the other side. This produces a highly asymmetric cranium and has allowed the fish to colonise and dominate benthic aquatic habitats (Evans et al, 2021). Directional asymmetry is also widespread in invertebrates (see Okumura et al, 2008;Pélabon and Hansen, 2008), including wing size and shape (Klingenberg et al, 1998;Pélabon and Hansen, 2008), body shape (e.g., the Chilean magnificent beetle (Ceroglossus chilensis); Bravi and Benítez, 2013, and Although it constitutes most of the examples in this study, directional asymmetry is by no means restricted to Animalia.…”

“…Asymmetry in the owl ear (both soft tissues and temporal parts of the skull, including modifications in the neurocranium and cartilaginous elements; Krings et al, 2020), serves to make the vertical directional sensitivity patterns different between the two ears for high frequencies, thus making possible vertical localization based on binaural comparison of intensity and spectral composition of sound (Norberg, 1977). Flatfishes (Pleuronectiformes) represent a diverse clade of benthic teleost fishes that possess a striking degree of cranial asymmetry exceeding that of any other vertebrate lineage (Black and Berendzen, 2020;Evans et al, 2021). The eyes of most flatfishes sit on the same side of the head; a development that happens during the larval stage where one eye of a symmetrical lava migrates to the other side.…”

The cichlid oral and pharyngeal jaws are evolutionarily and genetically coupled

“…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 . Indeed, there is an emerging consensus that phenotypic integration can facilitate rapid and coordinated trait evolution in teleosts 5 , 61 , 62 , and may reflect a general trend across organisms 4 , 63 , 64 . Within cichlids, a lack of functional integration between oral and pharyngeal jaws has enabled the separation of prey capture from prey processing, a mechanism that is considered key to their success 15 .…”

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

“…We found a small but significant effect of size in our shape data ( r 2 = 0.046 [SE = 0.002]; F = 12.419 [SE = 0.612]; p = 0.010 [SE = 0.001]). Given the relatively small effect of size on mandible shape and the observation that developmental and/or functional constraints on organismal shape may be a function of allometric scaling (Evans et al, 2021; Felice & Goswami, 2018; Marcy et al, 2020), we opted not to correct for allometry.…”