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Unweaving a hard taxonomic knot in coral reef dwellers: integrative systematics reveals two parallel cryptic species complexes in ‘marbled’ shrimps of the genus Saron Thallwitz 1891 (Caridea: Hippolytidae)

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Abstract

Phenotypic dissimilarity does not always evolve in concert with genetic diversification, resulting in cryptic species complexes that represent a major challenge for documenting actual biodiversity. Resolving these complexes is of paramount importance. Herein, we tested whether Saron marmoratus (Olivier, 1811) and S. neglectus de Man, 1902, two coral reef-dwelling shrimp species distributed over contiguous biogeographic provinces in the Indo-West Pacific and crossing various biogeographic and phylogeographic breaks, are such cryptic species complexes, as indicated by their significant diversity of color patterns. Firstly, a principal component analysis using 19 morphological traits confirmed that S. marmoratus and S. neglectus were morphologically distinctive, however, failing to detect morphologically defined groups within each of these taxa. On the other hand, molecular phylogenetic analyses (nuclear Histone 3 and mitochondrial 16S RNA markers) demonstrated a total of five well-supported clades in these two taxa, with moderate to deep genetic divergence among them. Species delimitation approaches indicated at least 10 (and a maximum of 15) putative cryptic species in the S. marmoratus and S. neglectus species complexes. Furthermore, color patterns segregated most but not all cryptic lineages. Altogether, the information above demonstrates that S. marmoratus and S. neglectus represent two cryptic species complexes, which diversified in somewhat parallel ways. Additional integrative studies, as we have shown here, to reveal the extend and magnitude of cryptic species complexes in coral reefs, are warranted given the current acute biodiversity crisis.

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Acknowledgements

We are most grateful to Gustav Paulay (FLMNH) and Laure Corbari (MNHN) for making material of Saron available for our study. We also thank Jean Lim for setting up the bGMYC package in the Palmetto Cluster at Clemson University. SP acknowledges United States India Educational Foundation (USIEF), New Delhi, and Fulbright Scholar Program, Washington, DC, for the award of a Fulbright-Nehru Post-Doctoral Research Fellowship (no. 2162/FNPDR/2016). This work was also financially supported from EU structural funding Operational Programme Research and Development for Innovation, project n. CZ.1.05/2.1.00/19.0388 (ZĎ), and from the Student grant project sgs/PřF/2020, University of Ostrava (PF). ZĎ and PF also acknowledge Ivona Horká and Eva Glincová (University of Ostrava) for additional molecular and/or biometric studies. A large part of the material studied herein was collected during several ‘Our Planet Reviewed’ expeditions, organized by the Muséum National d’Histoire Naturelle, Paris, France (MNHN). The Papua Niugini / Madang 2012 expedition (PIs: P. Bouchet, C. Payri and S. Samadi) was organized by the MNHN, Pro Natura International, Institut de Recherche pour le Développement, and University of Papua New Guinea (UPNG), with funding from the Total Foundation, Prince Albert II of Monaco Foundation, Foundation EDF, Stavros Niarchos Foundation and Entrepose Contracting, local support from the Divine Word University, and post-expedition support from Agence Nationale de la Recherche (ANR) and National Science Council of Taiwan (ANR-TF-DeepEvo 12 ISV7 005 01). The Papua Niugini / Kavieng 2014 expedition (PIs: P. Bouchet, J. Kinch, C. Payri) was organized by the MNHN and others (as above), with support from Papua New Guinea’s National Fisheries Authority, endorsement from the Nago Island Mariculture and Research Facility and New Ireland Provincial Administration, and with funding from the Total Foundation, the Laboratoire d’Excellence Diversités Biologiques et Culturelles (LabEx BCDiv, ANR-10-LABX-0003-BCDiv), the Programme Investissement d’Avenir (ANR-11-IDEX-0004-02), the Fonds Pacifique and CNRS INEE. Both Papua New Guinea expeditions operated under the Memorandum of Understanding with UPNG and permits delivered by the Papua New Guinea Department of Environment and Conservation. The Australian material was collected as part of several CReefs expeditions (Lizard Island, Heron Island, Ningaloo Reef), organized by Julian Caley (Australian Institute of Marine Science) and with participation of Slava Ivanenko, François Michonneau, Robert Lasley, one of the authors (ZĎ), and others. The French Polynesian material was collected under the Moorea Biocode project, based at the Richard B. Gump South Pacific research station of the University of Berkeley and sponsored by the Biocode Moorea project (http://www.mooreabiocode.org/) through the Gordon and Betty Moore Foundation; some Moorea material was collected by divers Gustav Paulay, Sea McKeon, Jenna Moore, Sarah McPherson, and Chris Meyer. The western Indian Ocean material was collected either as part of the BIOTAS project co-organized by the FLMNH (PI: G. Paulay) and the Université de la Réunion (PI: H. Bruggemann), or as part of a recent survey of the Djibouti reefs, with participation of G. Paulay. Finally, we thank all the photographers who kindly allowed us to use their excellent photographs: Andrey Rianskiy, Mark Strickland (www.markstrickland.com), Ned Deloach, Wei Tan, Gustav Paulay, and Tin-Yam Chan (National Taiwan Ocean University).

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Authors and Affiliations

  1. Department of Biological Sciences, Clemson University, Clemson, SC, 29634, USA

    J. Antonio Baeza

  2. Smithsonian Marine Station at Fort Pierce, 701 Seaway Drive, Fort Pierce, FL, 34949, USA

    J. Antonio Baeza

  3. Departamento de Biología Marina, Facultad de Ciencias del Mar, Universidad Católica del Norte, Larrondo 1281, Coquimbo, Chile

    J. Antonio Baeza

  4. Centre for Climate Change Studies, Sathyabama University, Rajiv Gandhi Salai, Chennai, Tamil Nadu, 600 119, India

    Sanjeevi Prakash

  5. Sathyabama Marine Research Station, 123 Sallimalai Street, Rameswaram, Tamil Nadu, 623526, India

    Sanjeevi Prakash

  6. Department of Biology and Ecology and Institute of Environmental Technologies, Faculty of Science, University of Ostrava, Chittussiho 10, 710 00, Ostrava, Czech Republic

    Pavlína Frolová & Zdeněk Ďuriš

  7. Universidade Federal de Goiás, Campus Samambaia, Instituto de Ciências Biológicas—ICB-5, Av. Esperança, S/N, Goiânia, Goiás, 74690-900, Brazil

    Arthur Anker

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JAB and AA were responsible for conceptualization, methodology, data curation, writing, original draft preparation, visualization, reviewing and editing. JAB, PS, PF, ZD, AA performed methodology, data curation, writing, reviewing and editing.

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Baeza, J.A., Prakash, S., Frolová, P. et al. Unweaving a hard taxonomic knot in coral reef dwellers: integrative systematics reveals two parallel cryptic species complexes in ‘marbled’ shrimps of the genus Saron Thallwitz 1891 (Caridea: Hippolytidae). Coral Reefs 42, 157–179 (2023). https://doi.org/10.1007/s00338-022-02317-9

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