Rates of morphological evolution, asymmetry and morphological integration of shell shape in scallops

Abstract

BackgroundRates of morphological evolution vary across different taxonomic groups, and this has been proposed as one of the main drivers for the great diversity of organisms on Earth. Of the extrinsic factors pertaining to this variation, ecological hypotheses feature prominently in observed differences in phenotypic evolutionary rates across lineages. But complex organisms are inherently modular, comprising distinct body parts that can be differentially affected by external selective pressures. Thus, the evolution of trait covariation and integration in modular systems may also play a prominent role in shaping patterns of phenotypic diversity. Here we investigate the role ecological diversity plays in morphological integration, and the tempo of shell shape evolution and of directional asymmetry in bivalved scallops.ResultsOverall, the shape of both valves and the magnitude of asymmetry of the whole shell (difference in shape between valves) are traits that are evolving fast in ecomorphs under strong selective pressures (gliders, recessers and nestling), compared to low rates observed in other ecomorphs (byssal-attaching, free-living and cementing). Given that different parts of an organism can be under different selective pressures from the environment, we also examined the degree of evolutionary integration between the valves as it relates to ecological shifts. We find that evolutionary morphological integration is consistent and surprisingly high across species, indicating that while the left and right valves of a scallop shell are diversifying in accordance with ecomorphology, they are doing so in a concerted fashion.ConclusionsOur study on scallops adds another strong piece of evidence that ecological shifts play an important role in the tempo and mode of morphological evolution. Strong selective pressures from the environment, inferred from the repeated evolution of distinct ecomorphs, have influenced the rate of morphological evolution in valve shape and the magnitude of asymmetry between valves. Our observation that morphological integration of the valves making up the shell is consistently strong suggests tight developmental pathways are responsible for the concerted evolution of these structures while environmental pressures are driving whole shell shape. Finally, our study shows that directional asymmetry in shell shape among species is an important aspect of scallop macroevolution.Electronic supplementary materialThe online version of this article (10.1186/s12862-017-1098-5) contains supplementary material, which is available to authorized users.

Morphological Diversification under High Integration in a Hyper Diverse Mammal Clade

“…In contrast, other studies identify clades with high rates of speciation and morphological evolution that are characterized by high levels of integration (Hu et al 2016;Sherratt et al 2017), possibly as a result of selection occurring along a single trajectory that may represent a line of least evolutionary resistance (Schluter 1996;Marroig and Cheverud 2005;Felice et al 2018). For example, Hu et al (2016) found high rates of speciation and morphological evolution coupled with high integration and neutral levels of disparity in icefish crania.…”

Phenotypic integration between claw and toepad traits promotes microhabitat specialization in the Anolis adaptive radiation

“…; Sherratt et al. ). Although claw loss has never been observed in anoles, dramatic claw reduction and even complete loss are observed in toepad‐bearing geckos (Russell and Bauer ; Khannoon et al.…”

“…Loss of function is common in traits that do not provide fitness benefits in particular populations or species (Fong et al 1995) and may explain the rapid evolutionary rate of claws, but not of toepads, in twig anoles (Tables 2 and 3; Fig. S3) through release from biomechanical constraint (Adams et al 2017a;Sherratt et al 2017). Although claw loss has never been observed in anoles, dramatic claw reduction and even complete loss are observed in toepad-bearing geckos (Russell and Bauer 2008; Khannoon et al 2015).…”

“…; Sherratt et al. ). Because traits that are under strong selection and biomechanical constraint often have lower rates of evolution (Adams et al.…”

“…Although another aspect of claw morphology, length, may acts as an extension of the toe in more terrestrial species, allowing for greater surface area contact and propulsive force when running on flat surfaces (Glen and Bennett 2007;Tulli et al 2009;Birn-Jeffery et al 2012), claw length does not affect clinging performance on any surface (Zani 2000;Tulli et al 2011) and, thus, should not be under correlative selection with toepad traits related to adhesive performance or other functionally relevant claw traits. Phenotypic integration is also expected to be linked to the rate of evolution across integrated traits (Frédérich et al 2014;Sherratt et al 2017). Because traits that are under strong selection and biomechanical constraint often have lower rates of evolution (Adams et al 2017a), sets of integrated biomechanical traits should evolve more slowly than those not under correlative selection.…”