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

Joanna M. Wolfe, Museum of Comparative Zoology and Department of Organismic & Evolutionary Biology, Harvard University, 26 Oxford St, Cambridge, MA 02138, USA.
Lauren Ballou, Institute of Environment and Department of Biological Sciences, Florida International University, Biscayne Bay Campus, North Miami, FL 33181, USA.
Javier Luque, Museum of Comparative Zoology and Department of Organismic & Evolutionary Biology, Harvard University, 26 Oxford St, Cambridge, MA 02138, USA.
Victoria M. Watson-Zink, Department of Biology, Stanford University, Stanford, CA 94305, USA.
Shane T. Ahyong, Australian Museum, 1 William St, Sydney, NSW 2010, Australia.
Joëlle Barido-Sottani, Institut de Biologie de l'École Normale Supérieure (IBENS), ENS, CNRS, INSERM, Université PSL (Paris Sciences & Lettres), Paris, France.
Tin-Yam Chan, Institute of Marine Biology and Center of Excellence for the Oceans, National Taiwan Ocean University, Keelung 202301, Taiwan, ROC.
Ka Hou Chu, Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China.
Keith A. Crandall, Computational Biology Institute, Department of Biostatistics and Bioinformatics, Milken Institute School of Public Health, George Washington University, Washington, DC 20052, USA.
Savel R. Daniels, Department of Botany and Zoology, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa.
Darryl L. Felder, Department of Invertebrate Zoology, US National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.
Harrison Mancke, Institute of Environment and Department of Biological Sciences, Florida International University, Biscayne Bay Campus, North Miami, FL 33181, USA.
Joel W. Martin, Research and Collections, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007, USA.
Peter K. Ng, Lee Kong Chian Natural History Museum, Faculty of Science, National University of Singapore, 2 Conservatory Drive, 117377 Singapore, Singapore.
Javier Ortega-Hernández, Museum of Comparative Zoology and Department of Organismic & Evolutionary Biology, Harvard University, 26 Oxford St, Cambridge, MA 02138, USA.
Emma Palacios Theil, Department of Invertebrate Zoology and Hydrobiology, University of Łódź, ul. Banacha 12/16, 90237 Łódź, Poland.
N Dean Pentcheff, Research and Collections, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007, USA.
Rafael Robles, Department of Biology and Laboratory for Crustacean Research, University of Louisiana at Lafayette, Lafayette, LA 70504, USA.
Brent P. Thoma, Department of Biology, Jackson State University, P.O. Box 18540, Jackson, MS 39217, USA.
Ling Ming Tsang, Simon F. S. Li Marine Science Laboratory, School of Life Sciences, The Chinese University of Hong Kong, Hong Kong SAR, China.
Regina Wetzer, Research and Collections, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, California 90007, USA.
Amanda M. Windsor, Department of Invertebrate Zoology, US National Museum of Natural History, Smithsonian Institution, Washington, DC 20560, USA.
Heather D. Bracken-Grissom, Institute of Environment and Department of Biological Sciences, Florida International University, Biscayne Bay Campus, North Miami, FL 33181, USA.

Document Type

Journal Article

Publication Date

11-6-2023

Journal

Systematic biology

DOI

10.1093/sysbio/syad066

Keywords

Brachyura; convergent evolution; crustaceans; divergence times; fossil calibration; molecular phylogeny; terrestrialization; threshold model

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 tips spanning 88 of 109 brachyuran 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 seven and up to 17 times convergently, and returned to the sea from non-marine environments at least twice. 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 extensive new 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.

Department

Biostatistics and Bioinformatics

Link to Full Text

Share

COinS