Convergent adaptation of true crabs (Decapoda: Brachyura) to a gradient of terrestrial environments

Abstract

For much of terrestrial biodiversity, the evolutionary pathways of adaptation from marine ancestors are poorly understood, and have usually been viewed as a binary trait. True crabs, the decapod crustacean infraorder Brachyura, comprise over 7,600 species representing a striking diversity of morphology and ecology, including repeated adaptation to non-marine habitats. Here, we reconstruct the evolutionary history of Brachyura using new and published sequences of 10 genes for 344 species spanning 88 of 104 families. Using 36 newly vetted fossil calibrations, we infer that brachyurans most likely diverged in the Triassic, with family-level splits in the late Cretaceous and early Paleogene. By contrast, the root age is underestimated with automated sampling of 328 fossil occurrences explicitly incorporated into the tree prior, suggesting such models are a poor fit under heterogeneous fossil preservation. We apply recently defined trait-by-environment associations to classify a gradient of transitions from marine to terrestrial lifestyles. We estimate that crabs left the marine environment at least five and up to 15 times convergently, and returned to the sea from non-marine environments three or four times. Although the most highly terrestrial- and many freshwater-adapted crabs are concentrated in Thoracotremata, Bayesian threshold models of ancestral state reconstruction fail to identify shifts to higher terrestrial grades due to the degree of underlying change required. Lineages throughout our tree inhabit intertidal and marginal marine environments, corroborating the inference that the early stages of terrestrial adaptation have a lower threshold to evolve. Our framework and newly compiled fossil and natural history datasets will enable future comparisons of non-marine adaptation at the morphological and molecular level. Crabs provide an important window into the early processes of adaptation to novel environments, and different degrees of evolutionary constraint that might help predict these pathways.

Fossil calibrations for molecular analyses and divergence time estimation for true crabs (Decapoda: Brachyura)

“…Despite the poor preservation of the holotype and sole specimen, the overall shape and fronto-orbital configuration match those of Ocypode. Thus, this occurrence from Argentina, together with those of Uca from Brazil and Afruca in Catalonia, indicate that Ocypodidae was already widespread by the mid-Miocene, and that the most recent common ancestor of Ocypodidae and its divergence from other thoracotremes must have occurred in the pre-Neogene, most likely in the Paleogene or even the Cretaceous (Wolfe et al, 2022).…”

“…As such, given the reliable systematic placement and the constrained stratigraphic age of Pinnixa sp. from the lower Miocene Culebra Formation in the Panama Canal Zone (Luque et al, 2017), this is to date the most reliable calibration datum for the crown group Pinnotheridae, while the most recent common ancestor of all extant pinnotherids must have originated in the pre-Neogene, most likely the Paleogene or Late Cretaceous (see Wolfe et al, 2022).…”

“…Molecular and morphological phylogenetics are key to better understanding the evolutionary relationships through common ancestry among and within brachyurans, allowing us to quantitatively examine previous views and hypotheses largely based on traditional alpha taxonomy. This is particularly important when considering problematic groups such as the so-called podotremes and the heterotreme eubrachyurans, now widely recognized as paraphyletic groups, as well as the relationships among primary freshwater groups (e.g., Tan et al, 2018;Wang et al, 2018;Luque et al, 2019b;Ma et al, 2019;Tang et al, 2020;Wang et al, 2020;Luque et al, 2021;Tsang et al, 2022;Wolfe et al, 2022;Zhang et al, 2022;Poore and Ahyong, 2023).…”

“…Such biases limit the number of remains than can fossilize, often restricted to the most resilient biomineralized body parts (e.g., claw dactyli and propodi remains), with whole organisms and soft to lightly-biomineralized tissues only preserved under exceptional conditions (Luque et al, 2021). These biases constrain the number of fossils suitable as reliable calibration points in molecular estimations of time divergence, and consequently the available fossil data that can be used to examine the evolution of terrestrialization and the transition from marine to non-marine habitats (Tsang et al, 2014;Luque et al, 2021;Watson-Zink, 2021;Tsang et al, 2022;Wolfe et al, 2022). Understanding the early origins of marine and nonmarine brachyurans by means of their fossil record requires not only new paleontological discoveries, but also a critical re-examination of previous records.…”

“…Here we present a set of 36 phylogenetically vetted fossil calibration points for molecular analyses and divergence time estimations of true crabs (one anomuran outgroup, 35 brachyuran ingroups) (based on the crown group topologies inferred by Wolfe et al, 2022) (Table 1), and provide information on the type of material investigated, its repository and catalogue number, phylogenetic justification, minimum and tip maximum ages, age justification, and a discussion, following best practices (Parham et al, 2012). For crown Meiura (Anomura + Brachyura)…”