Macroevolutionary patterns of body plan canalization in euarthropods

Abstract

Reconstructing patterns of macroevolution has become a central endeavor in paleobiology, because it offers insight into evolutionary models shaping the history of life. As the most diverse and abundant animals since the Cambrian period, arthropods provide copious data to elucidate the emergence of body plans in metazoan lineages. However, information provided by fossils on the tempo and mode of this phenomenon has lacked a recent synthesis. Here, I investigate macroevolutionary patterns of morphological evolution in Euarthropoda using a combined extinct and extant dataset optimized for multivariate analyses. Overall ordination patterns between the main morphogroups are consistent with another, independently coded, extant-only dataset providing molecular and morphological rates of evolution. Based on a “deep split” phylogenetic framework, total-group Mandibulata and Arachnomorpha emerge as directional morphoanatomical lineages, with basal fossil morphogroups showing heterogeneously spread-out occupations of the morphospace. In addition to a more homogeneous morphological variation, new morphogroups arose by successive reductions of translation distances; this pattern was interrupted only by terrestrialization events and the origin of pancrustaceans. A displaced optimum type of model is proposed to explain the fast assembly of canalized body plans during the Cambrian, with basal fossil morphogroups fitting intermediate fitness peaks in a moving adaptive landscape. Given time constraints imposed by the paleontological evidence, and owing to the interplay between canalization and modularity, as well as a decoupling between molecular and morphological rates, the rise of euarthropods would support the view that the swiftness of the Cambrian explosion was mostly associated with the buildup of genetic regulatory networks.

The origin and early evolution of arthropods

“…Correlative to this finding, and elaborating on previous phylogenetic results (Vannier et al 2018;Aria et al 2020), the iconic fuxianhuiids of the Chengjiang fauna (Figs 1, 2) have been described as mandibulates with strong morphological affinities with euthycarcinoids and myriapods (Aria et al 2021).…”

“…Parapeytoia). An alternative topology accommodating these issues is presented in a recent work (Aria 2020) as well as this paper (b) and is called "deep split," owing to the early branching of total-group Mandibulata and Arachnomorpha lineages. In this scenario, megacheirans are closer to chelicerates than they are to mandibulates, while hymenocarines are brought closer to the common euarthropod ancestor.…”

“…A variety of antero-dorsal and paired ventro-lateral sclerites mark the appearance of radiodontans, and their unique lateral elements may even constitute one of their strongest apomorphies (Van Roy et al 2015;Moysiuk and Caron 2019a;Cong et al 2017;Zeng et al 2018). Their continuity with arthropod carapaces and head shields is not entirely clear, but there is some evidence (Aria et al 2020) to posit that at least the antero-dorsal element, despite spanning a very large size range in radiodontans (Moysiuk and Caron 2019a), corresponds to the so-called "anterior/ocular sclerite" identified across early arthropods (Ortega-Hernández 2015; Aria and Caron 2017a), including megacheirans (Aria et al 2020) (Fig. 3b).…”

Exites in Cambrian arthropods and homology of arthropod limb branches

“…The evidence for homology of the lamellar exites in Megacheira ( Leanchoilia ) and Artiopoda ( Naraoia , Retifacies ) presented here suggests a single origin of this trait and accordingly, assuming that this trait is apomorphic, a close phylogenetic affinity between these taxa. Since both groups have been allied with chelicerates and both are recovered in some phylogenetic analyses in the chelicerate stem-group 35 , this character may serve as a synapomorphy of a clade within total-group Chelicerata. An alternative interpretation would be that this kind of exite is a symplesiomorphy, potentially retained from flaps bearing setal blades in stem-group arthropods such as Opabinia 39 .…”

“…Megacheira is resolved by character argumentation or quantitative phylogenetic analyses as either stem-group Euarthropoda 25 , 26 or as stem-group Chelicerata 27 – 30 . Trilobites and other artiopodans are alternatively allied to Mandibulata 31 – 34 or to Chelicerata 26 , 35 . The latter is consistent with the historical Arachnomorpha 36 , 37 or Lamellipedia 38 hypotheses, the latter named for lamellate setal blades in the exopodite.…”