Abstract
Many marine crustaceans form symbiotic relationships, yet there has been little work quantifying morphological adaptations in species specialized on different hosts. Here we examine morphological adaptations of symbiotic pea crabs (Pinnotheridae) to different host phyla. Multiple authors have noted that crabs living with burrowing hosts (burrowing shrimps and annelids) have different carapace shapes than species living with non-burrowing hosts (bivalves, gastropods, echinoderms, and ascidians), but this hypothesis has never been tested. Using digital analyses of taxonomic images, we calculated carapace aspect ratio of 149 pinnotherid species, and used phylogenetic ANOVA to test whether aspect ratio differed among species living with different hosts. Pea crab species living with burrowing hosts had significantly larger carapace aspect ratios (wide carapaces) than species living with non-burrowing hosts (round or square carapaces, or otherwise non-wider than long). Convergent evolution of morphological features in species with specialized host use may be a common—but understudied—pattern in many marine groups.
References
Anker A, Baeza JA (2012) Molecular and morphological phylogeny of hooded shrimps, genera Betaeus and Betaeopsis (Decapoda, Alpheidae): testing the center of origin biogeographic model and evolution of life history traits. Mol Phylo Evol 64:401–415
Appeltans W, Ahyong ST, Anderson G et al (2012) The magnitude of global marine species diversity. Curr Biol 22:2189–2202
Apprill A (2020) The role of symbioses in the adaptation and stress responses of marine organisms. Ann Rev Mar Sci 12:291–314
Atkins D (1926) The moulting stages of the pea-crab (Pinnotheres pisum). J Mar Biol Assoc UK 14:475–494
Baeza JA (1999) Indicadores de monogamia en el cangrejo commensal Pinnixa transversalis (Milne Edwards and Lucas)(Decapoda: Brachyura: Pinnotheridae): distribución poblacional, asociación macho-hembra y dimorfismo sexual. Rev Biol Mar Oceanogr 34(2):303–313
Baeza JA (2015) Crustaceans as symbionts: an overview of their diversity, host use and life styles. In: Thiel M, Watling L (eds) Lifestyles and feeding biology: the natural history of the Crustacea. Oxford University Press, Oxford, pp 163–189
Baker AC (2003) Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Ann Rev Ecol Evol Syst 34:661–689
Becker C, Türkay M (2010) Taxonomy and morphology of European pea crabs (Crustacea: Brachyura: Pinnotheridae). J Nat Hist 44:1555–1575
Becker C, Brandis D, Storch V (2011) Morphology of the female reproductive system of European pea crabs (Crustacea, Decapoda, Brachyura, Pinnotheridae). J Morph 272:12–26
Becker C, Klaus S, Tudge CC (2013) Male internal reproductive structures of European pea crabs (Crustacea, Decapoda, Brachyura, Pinnotheridae): Vas deferens morphology and spermatozoal ultrastructure. J Morph 274:1312–1322. https://doi.org/10.1002/jmor.20184
Bernays EA (1991) Evolution of insect morphology in relation to plants. Proc Roy Soc Lond B 1267:257–264
Bierbaum R, Shumway SE (1988) Filtration and oxygen consumption in mussels, Mytilus edulis, with and without pea crabs, Pinnotheres maculatus. Estuaries 11:264–271
Bolaños J, Cuesta JA, Hernández G, Hernández J, Felder DL (2004) Abbreviated larval development of Tunicotheres moseri (Rathbun, 1918)(Decapoda, Pinnotheridae), a rare case of parental care in brachyuran crabs. Sci Mar 68:373–384
Bruce A (1976a) Coral reef caridea and “commensalism.” Micronesica 12:83–98
Bruce A (1976b) Shrimps and prawns of coral reefs, with special reference to commensalism. In: Jones O, Endean R (eds) Biology and geology of coral reefs, vol 3. Academic Press, London, pp 37–94
Bush SE, Sohn E, Clayton DH (2006) Ecomorphology of parasite attachment: experiments with feather lice. J Parasitol 92:25–31
Campos E (2009) A new species and two new genera of pinnotherid crabs from the northeastern Pacific Ocean, with a reappraisal of the subfamily Pinnotherinae de Haan, 1833 (Crustacea: Brachyura: Pinnotheridae). Zootaxa 2022:29–44
Campos E (2013) Remarks on the sexual dimorphism and taxonomy of Fabia Dana, 1851 (Crustacea, Brachyura, Pinnotheridae). Zootaxa 3616:190–200
Campos E (2016) The Pinnotheridae of the northeastern Pacific (Alaska to Mexico): zoogeographical remarks and new bivalve hosts (Crustacea, Brachyura, Pinnotheridae). Zootaxa 4170:311–329
Castro P (2015) Symbiotic brachyura. In: Treatise on zoology: anatomy, taxonomy, biology the Crustacea, Volume 9 Part C. Brill, pp 543–581
Chow LH, De Grave S, Tsang LM (2021) Evolution of protective symbiosis in palaemonid shrimps (Decapoda: Caridea) with emphases on host spectrum and morphological adaptations. Mol Phylo Evol 162:107201
Costello MJ, Coll M, Danovaro R, et al (2010) A census of marine biodiversity knowledge resources, and future challenges. PLoS ONE 5:e12110
Cuesta JA, Raso J, Abello P et al (2019) A new species of pea crab from south-western Europe (Crustacea, Decapoda, Brachyura): species description, geographic distribution and population structure with an identification key to European Pinnotheridae. J Mar Biol Assoc UK 99:1141–1152
Darriba D, Taboada GL, Doallo R et al (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772–772
De Bruyn C, Rigaud T, David B et al (2009) Symbiosis between the pea crab Dissodactylus primitivus and its echinoid host Meoma ventricosa: potential consequences for the crab mating system. Mar Ecol Prog Ser 375:173–183. https://doi.org/10.3354/meps07733
De Bryun C, David B, De Ridder C et al (2010) Asymmetric exploitation of two echinoid host species by a parasitic pea crab and its consequences for the parasitic life cycle. Mar Ecol Prog Ser 398:183–191. https://doi.org/10.3354/meps08315
de Gier W, Becker C (2020) A review of the ecomorphology of pinnotherine pea crabs (Brachyura: Pinnotheridae), with an updated list of symbiont-host associations. Diversity 12:431
Drummond A, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214
Ďuriš Z, Horká I, Juračka PJ, et al (2011) These squatters are not innocent: the evidence of parasitism in sponge-inhabiting shrimps. PLoS ONE 6:e21987
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nuc Acids Res 32:1792–1797
Felder DL, Palacios Theil E (2020) A new pinnotherid crab of the genus Pinnixulala Palacios Theil, Cuesta and Felder, 2016 from uncertain infaunal hosts in the northern Gulf of Mexico, with a rediagnosis and updated synonymy for the polychaete symbiont Pinnixulala retinens (Rathbun, 1918) (Decapoda: Brachyura: Pinnotheridae). J Crust Biol 40(6):887–898. https://doi.org/10.1093/jcbiol/ruaa063
Fransen CHJM (2002) Taxonomy, phylogeny, historical biogeography, and historical ecology of the genus Pontonia (Crustacea: Decapoda: Caridea: Palaemonidae). Zool Verhan 336:1–433
Garland T, Dickerman AW, Janis CM et al (1993) Phylogenetic analysis of covariance by computer simulation. Syst Biol 42:265–292
Guimaraes P, Rico-Gray V, dos Reis S et al (2006) Asymmetries in specialization in ant-plant mutualistic networks. Proc Roy Soc B Biol Sci 273:2041–2047
Hamel JF, Ng PK, Mercier A (1999) Life cycle of the pea crab Pinnotheres halingi sp nov, an obligate symbiont of the sea cucumber Holothuria scabra Jaeger. Ophelia 50:149–175
Harnos A, Lang Z, Petrás D et al (2017) Size matters for lice on birds: coevolutionary allometry of host and parasite body size. Evolution 71:421–431
Harrison JS (2004) Evolution, biogeography, and the utility of mitochondrial 16s and COI genes in phylogenetic analysis of the crab genus Austinixa (Decapoda: Pinnotheridae). Mol Phylo Evol 30:743–754
Hines AH (1992) Constraint on reproductive output in brachyuran crabs: pinnotherids test the rule. Am Zool 32:503–511
Horká I, De Grave S, Fransen CHJM et al (2018) Multiple origins and strong phenotypic convergence in fish-cleaning palaemonid shrimp lineages. Mol Phylo Evol 124:71–81
Hultgren KM, Duffy JE (2010) Sponge host characteristics shape the community structure of their shrimp associates. Mar Ecol Prog Ser 407:1–12
Hurt C, Hultgren KM, Anker A, Lemmon AR, Lemmon EM, Bracken-Grissom H (2021) First worldwide molecular phylogeny of the morphologically and ecologically hyperdiversified snapping shrimp genus Alpheus (Malacostraca: Decapoda). Mol Phylo Evol 158:107080
Johnson KP, Shreve SM, Smith VS (2012) Repeated adaptive divergence of microhabitat specialization in avian feather lice. BMC Biol 10:52–11
Jossart Q, Wattier RA, Kastally C et al (2014) Genetic evidence confirms polygamous mating system in a crustacean parasite with multiple hosts. PLoS ONE 93(3):e90680. https://doi.org/10.1371/journal.pone.0090680
Jossart Q, De Ridder C, Lessios HA et al (2017) Highly contrasted population genetic structures in a host-parasite in the Caribbean Sea. Ecol Evol 7(22):9267–9280. https://doi.org/10.1002/ece3.3413
Jossart Q, Terrana L, De Ridder C et al (2020) To see or to smell: the role of vision in host-recognition by an ectoparasitic crab. Symbiosis 80:97–101. https://doi.org/10.1007/s13199-019-00657-9
Kane K, Farley GS (2006) Body size of the endosymbiotic pea crab Tumidotheres maculatus: larger hosts hold larger crabs. Gulf Caribbean Res 18:27–34
Kays R, McShea WJ, Wikelski M (2020) Born-digital biodiversity data: millions and billions. Div Distrib 26:644–648
Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464
Manning RB (1993) West African pinnotherid crabs, subfamily Pinnotherinae (Crustacea, Decapoda, Brachyura). Bull Muséum D’hist Nat 15:125–177
Manning RB, Felder DL (1989) The Pinnixa cristata complex in the Western Atlantic with a description of two new species (Crustacea: Decapoda: Pinnotheridae). Smithsonian Contrib Zool 1–36
Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogenetic trees. Proc Gateway Comp Environ Workshop (GCE):1–8
Møller Christensen A, McDermott JJ (1958) Life-history and biology of the oyster crab, Pinnotheres ostreum Say. Biol Bull 114:146–179
Mora C, Tittensor DP, Adl S et al. (2011) How many species are there on earth and in the ocean? PLoS Biol 9:e1001127
Morand S, Hafner MS, Page RD, Reed DL (2000) Comparative body size relationships in pocket gophers and their chewing lice. Biol J Linn Soc 70:239–249
Mugleston JD, Song H, Whiting MF (2013) A century of paraphyly: a molecular phylogeny of katydids (Orthoptera: Tettigoniidae) supports multiple origins of leaf-like wings. Mol Phylo Evol 69:1120–1134
Ng PKL, Meyer C (2016) A new species of pea crab of the genus Serenotheres Ahyong and Ng, 2005 (Crustacea, Brachyura, Pinnotheridae) from the date mussel Leiosolenus Carpenter, 1857 (Mollusca, Bivalvia, Mytilidae, Lithophaginae) from the Solomon Islands. Zookeys 623:31–41. https://doi.org/10.3897/zookeys.623.10272
Nylander J, Ronquist F, Huelsenbeck J et al (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67
Ocampo EH, Nuñez JD, Cledón M, Baeza JA (2012) Host-specific reproductive benefits host selection behavior and host use pattern of the pinnotherid crab Calyptraeotheres garthi. J Exp Mar Biol Ecol 429:36–46
Ocampo EH, Robles R, Terossi M et al (2013) Phylogeny, phylogeography, and systematics of the American pea crab genus Calyptraeotheres Campos, 1990, inferred from molecular markers. Zool J Linn Soc 169:27–42
Ocampo EH, Nuñez JD, Cledón M, Baeza JA (2014) Parasitic castration in slipper limpets infested by the symbiotic crab Calyptraeotheres garthi. Mar Biol 161:2107–2120
Ocampo EH, Luppi TA, Spivak ED, Klaus S (2018) The ontogeny of the female reproductive system in the parasitic castrator pea crab Calyptraeotheres garthi: implications for its mating system. J Morphol 279:531–544
Palacios Theil E (1993) Felder DL (2019) Molecular phylogeography of Tumidotheres maculatus (Say, 1818) and Zaops ostreum (Say, 1817) (Crustacea: Decapoda: Pinnotheridae) in the western Atlantic, with description of a new species and synonymy of Epulotheres Manning. Mar Biol Res 15(10):548–567. https://doi.org/10.1080/17451000.2019.1693597
Palacios Theil E, Felder DL (2020) Phylogeny of the genus Austinixa Heard and Manning, 1997 inferred from mitochondrial and nuclear molecular markers, with descriptions of three new species and redescription of Austinixa felipensis (Glassell, 1935)(Decapoda: Brachyura: Pinntoheridae). Zootaxa 4778(1):101–134. https://doi.org/10.11646/zootaxa.4778.1.4
Palacios Theil E, Cuesta JA, Felder DL (2016) Molecular evidence for non-monophyly of the pinnotheroid crabs (Crustacea: Brachyura: Pinnotheroidea), warranting taxonomic reappraisal. Invert Syst 30:1–27
Pearce B (1964) On reproduction in Pinnotheres maculatus (Decapoda: Pinnotheridae). Biol Bull 127:384
Pearce JB (1966b) The biology of the mussel crab, Fabia subquadrata, from the waters of the San Juan Archipelago, Washington. Pac Sci 20:3–35
Pearce JB (1966a) On Pinnixa faba and Pinnixa littoralis (Decapoda: Pinnotheridae) symbiotic with the clam, Tresus capax (Pelecypoda: Mactridae) In: Barnes H (ed) Some contemporary studies in marine science. George Allen and Unwin Ltd., London, pp. 565–589
Peiró DF, Baeza JA, Mantelatto FL (2013) Host-use pattern and sexual dimorphism reveals the mating system of the symbiotic pea crab Austinixa aidae (Crustacea: Brachyura: Pinnotheridae). J Mar Biol Assoc UK 93:715–723
R Core Team (2020) R: A language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. www.R-project.org
Rambaut A, Drummond AJ, Xie D, et al (2018) Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901
Raupach MJ, Barco A, Steinke D et al (2015) The application of DNA barcodes for the identification of marine crustaceans from the North Sea and adjacent regions. PLoS ONE 10:e0139421-e139423
Revell LJ (2012) phytools: an R package for phylogenetic comparative biology (and other things). Meth Ecol Evol 3:217–223
Revell LJ (2013) Two new graphical methods for mapping trait evolution on phylogenies. Meth Ecol Evol 4:754–759
Ronquist F, Teslenko M, van der Mark P et al (2012) MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542
Rudy P, Rudy LH, Watson JF (2013) Oregon estuarine invertebrates: an illustrated guide to the common and important invertebrate animals. Fish and Wildlife Service
Ruxton GD, Allen WL, Sherratt TN, Speed MP (2018) Avoiding attack: the evolutionary ecology of crypsis aposematism, and mimicry. Oxford University Press, Oxford
Schmitt W, McCain J, Davidson E (1973) Decapoda I Brachyura I Family Pinnotheridae. In: Gruner H, Holthuis LB (eds) Crustaceorum Catalogus (Vol 3) Crustaceorum Catalogus
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Meth 9:671–675
Stecher G, Tamura K, Kumar S (2020) Molecular evolutionary genetics analysis (MEGA) for macOS. Mol Biol Evol 1237–1239.
Watanabe T, Henmi Y (2009) Morphological development of the commensal pea crab (Arcotheres sp) in the laboratory reared specimens. J Crust Biol 29:217–223
Wells WW (1928) Pinnotheridae of puget sound. Pub Puget Sound Biol Station 6:283–314
Wells HW, Wells MJ (1961) Observations on Pinnaxodes floridensis, a new species of pinnotherid crustacean commensal in holothurians. Bull Mar Sci 11:267–279
WoRMS Editorial Board (2021) World register of marine species. http://www.marinespecies.org at VLIZ. Accessed 2021–03–01 doi:1014284/170
Zmarzly DL (1992) Taxonomic review of pea crabs in the genus Pinnixa (Decapoda: Brachyura: Pinnotheridae) occurring on the California shelf, with descriptions of two new species. J Crust Biol 12:677–713
Acknowledgements
We would like to thank the librarians at Seattle University for assisting with an endless stream of requests for taxonomic literature, and Charles Lewis for assisting with some shape measurements. Carla Hurt gave very useful comments on an earlier draft of the paper, and Ernesto Campos and an anonymous reviewer made several suggestions that greatly improved the quality of the final manuscript. Finally, we owe a debt of gratitude to the myriad of talented taxonomists and pea crab workers who produced the images used in this study.
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Hultgren, K.M., Foxx, C.L. & Palacios Theil, E. Host-associated morphological convergence in symbiotic pea crabs. Evol Ecol 36, 273–286 (2022). https://doi.org/10.1007/s10682-022-10153-0
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DOI: https://doi.org/10.1007/s10682-022-10153-0