Diversification and distribution of gall crabs (Brachyura: Cryptochiridae: Opecarcinus) associated with Agariciidae corals

Coral reefs are home to the greatest diversity of marine life, and many species on reefs live in symbiotic associations. Studying the historical biogeography of symbiotic species is key to unravelling (potential) coevolutionary processes and explaining species richness patterns. Coral-dwelling gall crabs (Cryptochiridae) live in obligate symbiosis with a scleractinian host, and are ideally suited to study the evolutionary history between heterogeneous taxa involved in a symbiotic relationship. The genus Opecarcinus Kropp and Manning, 1987, like its host coral family Agariciidae, occurs in both Indo-Pacific and Caribbean seas, and is the only cryptochirid genus with a circumtropical distribution. Here, we use mitochondrial and nuclear DNA gene fragments of Opecarcinus specimens sampled from 21 Indo-Pacific localities and one Atlantic (Caribbean) locality. We applied several species delimitation tests to characterise species diversity, inferred a Bayesian molecular-clock time-calibrated phylogeny to estimate divergence times and performed an ancestral area reconstruction. Time to the most recent common ancestor (tMRCA) of Opecarcinus is estimated at 15−6 Mya (middle Miocene—late Miocene). The genus harbours ~ 15 undescribed species as well as several potential species complexes. There are indications of strict host-specificity patterns in certain Opecarcinus species in the Indo-Pacific and Atlantic, however, a robust phylogeny reconstruction of Agariciidae corals—needed to test this further—is currently lacking. The Indo-West Pacific was inferred to be the most probable ancestral area, from where the Opecarcinus lineage colonised the Western Atlantic and subsequently speciated into O. hypostegus. Opecarcinus likely invaded from the Indo-West Pacific across the East Pacific Barrier to the Atlantic, before the full closure of the Isthmus of Panama. The subsequent speciation of O. hypostegus, is possibly associated with newly available niches in the Caribbean, in combination with genetic isolation following the closure of the Panama Isthmus.

Citation

Xu, T., Bravo, H., Paulay, G., & van der Meij, S. E. T. (2021). Diversification and distribution of gall crabs (Brachyura: Cryptochiridae: Opecarcinus) associated with Agariciidae corals. Coral Reefs. doi:10.1007/s00338-021-02163-1

Sponsors

We thank Francesca Benzoni (KAUST) for providing background information on the systematics of the Agariciidae, and Jorn Claassen (RUG) for help with BioGeoBEARS. The fieldwork in Indonesia was organised by Naturalis and the Research Centre for Oceanography (RCO-LIPI), under the umbrella of Ekspedisi Widya Nusantara (E-Win). We are grateful to LIPI and RISTEK for granting research permits. The fieldwork in Malaysia was WWF-Malaysia, Universiti Malaysia Sabah's Borneo Marine Research Institute, and Universiti Malaya's Institute of Biological Sciences, Sabah Parks and funded through WWF-Malaysia, the Ministry of Science, Technology and Innovation (MOSTI) and USAID CTSP (Coral Triangle Support Partnership). The research permits were granted by the Economic Planning Unit, Prime Minister's Department and Sabah Biodiversity Centre. Collecting in New Caledonia was done during the mission CORALCAL 4. Provinces Sud and Nord of New Caledonia provided sampling permits. Loyalty Island samples were collected during the BIBELOT campaign in 2014 onboard RV Alis of IRD at Nouméa. Sampling permits were granted by the Loyalty Islands Province, New Caledonia. For the samples from the Maldives, the help of the University of Milano-Bicocca Marine Research and High Education Centre in Magoodhoo, the Ministry of Fisheries and Agriculture, Republic of Maldives, and the community of Magoodhoo, Faafu Atoll is gratefully acknowledged. Fieldwork in the Red Sea was supported by the King Abdullah University of Science and Technology under the Biodiversity in the Saudi ArabianRed Sea program, award number CRG-1-BER-002 to Michael Berumen. Support for the various fieldwork trips by SETM was provided by Van Tienhoven Foundation for International Nature Protection, Stichting Fonds C. Tussenbroek (Nell Ongerboerfonds), Academy Ecology Fund (KNAW), LUF International Study Fund (Leiden University), TREUB-maatschappij, L.B. Holthuisfonds, J.-J. ter Pelkwijkfonds, and A. M. Buitendijkfonds. We are also grateful for the scholarship of TX, provided by the China Scholarship Council (CSC), and NSF DEB 1856245 for funding GP.