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Type: Article
Published: 2019-07-29
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Widespread phenotypic hypervariation in the enigmatic anchialine shrimp Barbouria cubensis (Decapoda: Barbouriidae)

3000 NE 151st St., MSB 330, North Miami, FL 33181.
210501 FGCU Blvd. South, WH 118 Fort Myers, FL 33965.
10501 FGCU Blvd. South, WH 118 Fort Myers, FL 33965.
3000 NE 151st St., MSB 330, North Miami, FL 33181.
Crustacea molecular barcoding taxonomy cave shrimp Bahamas Atlantic phylogeny barbouriid species

Abstract

Classification and evolutionary relationships among anchialine shrimp from the family Barbouriidae Christoffersen, 1987, has long been a topic of debate amongst crustacean taxonomists. To date, no study has examined morphological or molecular variation among populations of these enigmatic shrimp. The present study documents and analyzes patterns of widespread morphological variation within populations of Barbouria cubensis von Martens, 1872, from anchialine pools on three Bahamian islands. Such extensive morphological variation confounds identification using classic taxonomical methods. Phenotypic variation is by no means a new topic, but studies of decapods are typically limited to isolated individuals or few morphological characters. Moreover, past studies of B. cubensis do not report extensive morphological variation, however we find that upwards of 90% of individuals are affected. Anomalous phenotypes are described in 54 morphological characters with no detectable pattern associated with geographic distribution. The term phenotypic hypervariation (PhyV) is used to describe morphological variation that greatly deviates from any previous taxonomic descriptions.  Analysis of partial sequences of the 16S and COI mitochondrial genes confirm the identity of morphologically variable specimens as B. cubensis without population structure across the tropical western Atlantic. A test for cryptic diversity within B. cubensis suggests PhyV is not correlated with cryptic diversity. Morphological variation at this scale likely depends on recent changes either to their environment or genetic diversity.

 

References

  1. Agnalt, A.L., Grefsrud, E.S., Farestveit, E., Larsen, M. & Keulder, F. (2013) Deformities in larvae and juvenile European lobster (Homarus gammarus) exposed to lower pH at two different temperatures. Biogeosciences, 10, 7883–7895.

    https://doi.org/10.5194/bg-10-7883-2013

    Ahyong, S. & O’ Meally, D. (2004) Phylogent of the Decapoda Reptantia: Resolution using three molecular loci and morphology. The Raffles Bulletin of Zoology, 52, 673–693.

    Allegue, H., Araya-Ajoy, Y.G., Dingemanse, N.J., Dochtermann, N.A., Garamszegi, L.Z., Nakagawa, S., Réale, D., Schielzeth, H. & Westneat, D.F. (2017) Statistical Quantification of Individual Differences (SQuID): an educational and statistical tool for understanding multilevel phenotypic data in linear mixed models. Methods in Ecology and Evolution, 8, 257–267.

    https://doi.org/10.1111/2041-210X.12659

    Agrawal, A.A. (2001) Phenotypic plasticity in the interactions and evolution of species. Science, 294 (5541), 321–326.

    https://doi.org/10.1126/science.1060701

    Aguirre, H. & Hendrickx, M.E. (2005) Abnormal rostrum and telson in two species of Penaeid shrimp (Decapoda, Dendrobranchiata, Penaeidae) from the Pacific coast of Mexico. Crustaceana, 78 (1), 113–119.

    https://doi.org/10.1163/1568540054024501

    Aznar-Cormano, L., Brisset, J., Chan, T.Y., Corbari, L., Puillandre, N., Utge, J., Zbinden, M., Zuccon, D. & Samadi, S. (2015) An improved taxonomic sampling is a necessary but not sufficient condition for resolving inter-families relationships in Caridean decapods. Genetica, 143, 195–205.

    https://doi.org/10.1007/s10709-014-9807-0

    Baeza, J.A. (2013) Molecular phylogeny of broken-back shrimps (genus Lysmata and allies): A test of the ‘Tomlinson-Ghiselin’ hypothesis explaining the evolution of hermaphroditism. Molecular Phylogenetics and Evolution, 69, 46–62.

    https://doi.org/10.1016/j.ympev.2013.05.013

    Baltanás, A., Alcorlo, P. & Danielopol, D.L. (2002) Morphological disparity in populations with and without sexual reproduction: a case study in Eucypris virens (Crustacea: Ostracoda). Biological Journal of the Linnean Society, 75, 9-19.

    https://doi.org/10.1046/j.1095-8312.2002.00001.x

    Bauer, R.T. (2005) 7 Library of Congress Cataloging-In-Publication Data Remarkable Shrimps: Adaptations and Natural History of the Carideans. Animal nat. V.H. Hutchison (Ed.), University of Oklahoma Press: Norman, Norman, Ok.

    Becking, L.E., Renema, W., Santodomingo, N.K., Hoeksema, B.W., Tuti, Y. & de Voogd, N.J. (2011) Recently discovered landlocked basins in Indonesia reveal high habitat diversity in anchialine systems. Hydrobiologia, 677 (1), 89–105.

    https://doi.org/10.1007/s10750-011-0742-0

    Béguer, M., Feuillassier, L., Elie, P., Boët P. & Giradin, M. (2010) Exoskeletal deformities in Palaemonidae: are they a threat to survival?. Marine Environmental Research, 69 (3), 109–117.

    https://doi.org/10.1016/j.marenvres.2009.09.001

    Béguer, M., Pasquaud S., Noël, P. Girardin, M. & Boët, P. (2008) First description of heavy skeletal deformations in Palaemon shrimp populations of European estuaries: the case of the Gironde (France). Hydrobiologia, 607, 225–229.

    https://doi.org/10.1007/s10750-008-9386-0

    Bishop, R.E., Humphreys, W.F., Cukrov, N., Žic, V., BOXSHALL, G.A., Cukrov, M., Iliffe, T.M., Kršinić, F., Moore, W.S., Pohlman, J.W., Sket, B., Bishop, R.E., Kršinić, F., Sket, B., Iliffe, T.M., Žic, V., Moore, W.S., Cukrov, N., Cukrov, M., BOXSHALL, G.A. & Pohlman, J.W. (2015) ‘Anchialine’ redefined as a subterranean estuary in a crevicular or cavernous geological setting. Journal of Crustacean Biology, 35 (4), 511–514.

    https://doi.org/10.1163/1937240X-00002335

    Bishop, R.E. & Iliffe, T.M. (2012) Ecological physiology of the anchialine shrimp Barbouria cubensis: a comparison of epigean and hypogean populations. Marine Biodiversity, 42, 303–310.

    https://doi.org/10.1007/s12526-012-0113-8

    Bohonak, A.J. (1999) Dispersal, Gene Flow, and Population Structure. The Quarterly Review of Biology, 74 (1), 21–45.

    https://doi.org/10.1086/392950

    Borradaile, L.A. (1900) On some Crustaceans from the South Pacific. Part IV. The crabs. Proceedings fo the General Meetings for the Scientific Business of the Zoological Society of London, 1900 (3), 568–596.

    Bracken-Grissom, H.D., Ahyong, S.T., Wilkinson, R.D., Feldmann, R.M., Schweitzer, C.E., Breinholt, J.W., Bendall, M., Palero, F., Chan, T.-Y., Felder, D.L., Robles, R., Chu, K.-H., Tsang, L.-M., Kim, D., Martin, J.W. & Crandall, K.A. (2014) The emergence of the lobsters: phylogenetic relationships, morphological evolution and divergence time comparisons of an ancient group (Decapoda: Achelata, Glypheidea, Polychelida). Systematic Biology, 63, 457–479.

    https://doi.org/10.1093/sysbio/syu008

    Bracken, H.D., Toon, A, Felder, D.L., Martin, J.W., Finley, M., Rasmussen, J., Palero, F. & Crandall, K. (2009) The decapod tree of life: compiling the data and moving toward a consensus of decapod evolution. Arthropod Systematics and Phylogeny, 67, 99–116.

    Brandt, A. (1988) Morphology and Ultrastructure of the Sensory Spine, a Presumed Mechanoreceptor of Sphaerome hookeri (Crustacea, Isopods), and Remarks on Similar Spines in Other Peracarids. Journal of Morphology, 198, 219–229.

    https://doi.org/10.1002/jmor.1051980208

    Brian, J. V., Fernandes, T., Ladle, R.J. & Todd, P.A. (2006) Patterns of morphological and genetic variability in UK populations of the shore crab, Carcinus maenas Linnaeus, 1758 (Crustacea: Decapoda: Brachyura). Journal of Experimental Marine Biology and Ecology, 329 (1), 47–54.

    https://doi.org/10.1016/j.jembe.2005.08.002

    Chace, F.A. (1997) The Caridean Shrimps (Crustacea: Decapoda) of the Albatross Philippine Expedition, 1907–1910, part 7: families Atyidae, Eugonatonotidae, Rhynchocinetidae, Bathypalaemonellidae, Processidae, and Hippolytidae. Smithsonian Contributions to Zoology, 587, 1–106.

    https://doi.org/10.5479/si.19436696.391.1

    Chace, F.A. (1972) The shrimps of the Smithsonian-Bredin Caribbean Expeditions with a summary of the West Indian shallow-water species (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology, 98, 1–179.

    https://doi.org/10.5479/si.00810282.98

    Chace, F.A. & Manning, R.B. (1972) Two new caridean shrimps, one representing a new family, from marine pools on Ascension Island (Crustacea: Decapoda: Natantia). Smithsonian Contributions to Zoology, 1–18.

    https://doi.org/10.5479/si.00810282.131

    Chown, S.L., Slabber, S., McGeouch, M., Janion, C. & Leinaas, H.P. (2007) Phenotypic plasticity mediates climate change responses among invasive and indigenous arthropods. Proceedings of Biological sciences, 274 (1625), 2531–2537.

    https://doi.org/10.1098/rspb.2007.0772

    Christoffersen, M.L. (1987) Phylogenetic Relationships of Hippolytid Genera, with an Assignment of New Families for the Crangonoidea and Alpheoidea (Crustacea, Decapoda, Caridea). Cladistics, 3 (4), 348–362.

    https://doi.org/10.1111/j.1096-0031.1987.tb00898.x

    Clark, J. (1989) Koror misticius, new genus, new species (Decapoda: Hippolytidae), a cave shrimp from Palau. Journal of Crustacean Biology, 9 (3), 445–452.

    https://doi.org/10.2307/1548569

    Cockayne, L. & Allan, H.H. (1926) The Naming of Wild Hybrid Swarms. Nature, 118 (2974), 623–624.

    https://doi.org/10.1038/118623a0

    Cornils, A. & Held, C. (2014) Evidence of cryptic and pseudocryptic speciation in the Paracalanus parvus species complex (Crustacea, Copepoda, Calanoida). Frontiers in Zoology, 11 (19), 1–17.

    https://doi.org/10.1186/1742-9994-11-19

    Crandall, K.A., Fitzpatrick, J.F., Biology, S. & Mar, N. (1996) Crayfish Molecular Systematics: Using a Combination of Procedures to Estimate Phylogeny. Systematic Biology, 45, 1–26.

    https://doi.org/10.1093/sysbio/45.1.1

    Cristescu, M.E., Adamowicz, S.J., Vaillant, J.J. & Haffner, D.G. (2010) Ancient lakes revisited: From the ecology to the genetics of speciation. Molecular Ecology, 19 (22), 4837–4851.

    https://doi.org/10.1111/j.1365-294X.2010.04832.x

    Dawson, M.N. (2005) Incipient speciation of Catostylus mosaicus (Scyphozoa, Rhizostomeae, Catostylidae), comparative phylogeography and biogeography in south-east Australia. Journal of Biogeography, 32 (3), 515–533.

    https://doi.org/10.1111/j.1365-2699.2004.01193.x

    DeWitt, T.J., Robinson, B.W. & Wilson, D.S. (2000) Functional diversity among predators of a freshwater snail imposes an adaptive trade-off for shell morphology. Evolutionary Ecology Research, 2, 129–148.

    De Grave, S., Li, C.P., Tsang, L.M., Chu, K.H. & Chan, T.Y. (2014) Unweaving hippolytoid systematics (Crustacea, Decapoda, Hippolytidae): Resurrection of several families. Zoologica Scripta, 43, 496–507.

    https://doi.org/10.1111/zsc.12067

    De Grave, S., Pentcheff, N.D., Ahyong, S.T., Chan, T., Crandall, K.A., Dworschak, P.C., Felder, D.L., Feldmann, R.M., Fransen, C.H.J.M., Goulding, L.Y.D., Lemaitre, R., Low, M.E.Y., Martin, J.W., Ng, P.K.L., Schweitzer, C.E., Tan, S.H., Tshudy, D. & Wetzer, R. (2009) A classification of living and fossil genra of decapod crustaceans. Raffles Bulltein of Zoology, 21, 1–109.

    Duarte, M.S., Maia-Lima, F.A. & Molina, W.F. (2008) Interpopulational morphological analyses and fluctuating asymmetry in the brackish crab Cardisoma guanhumi Latreille (Decapoda, Gecarcinidae), on the Brazilian Northeast coastline. Pan-American Journal of Aquatic Sciences, 3 (3), 294–303.

    Edwards, D.C. (1996) The inland saline waters of the Bahamas as distinctive scientific resources. In: Proceedings of the Sixth Symposium on Natural History of the Bahamas, pp. 152–162.

    Felsenstein, J. & Churchill, G.A. (1996) A hidden Markov model approach to variation among sites in rate of evolution. Molecular Biology and Evolution, 13, 93–104.

    https://doi.org/10.1093/oxfordjournals.molbev.a025575

    Fernandes, C.M., Gregati R.A. & Bichuette M.E. (2011) The frist record of external abnormalities in the subterranean Aegla marginata Bond-Buckup & Buckup, 1994 (Crustacea: Decapoda: Aeglidae), from a karst area of Southeastern Brazil. Subterranean Biology, 8, 33–38.

    https://doi.org/10.3897/subtbiol.8.1228

    Fiedler, G.C., Rhyne, A.L., Segawa, R., Aotsuka, T. & Schizas, N.V. (2010) The evolution of euhermaphroditism in caridean shrimps: a molecular perspective of sexual systems and systematics. BMC Evolutionary Biology, 10 (297), 14 pp.

    https://doi.org/10.1186/1471-2148-10-297

    Follesa, M.C., Cannas, R., Gastoni, A., Cabiddu, S. Deiana, A.M. & Cau A. (2008) Abnormal rostrum in Polycheles typhlops Heller, 1862 (Decapoda: Polychelidae) from the Central Western Mediterranean. Journal of Crustacean Biology, 28 (4), 731–734.

    https://doi.org/10.1651/08-2987.1

    Folmer, O., Black, M., Hpeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3, 294–299.

    Fumagalli, L., Snoj, A., Jesenšek, D., Balloux, F., Jug, T., Duron, O., Brossier, F., Crivelli, A.J. & Berrebi, P. (2002) Extreme genetic differentiation among the remnant populations of marble trout (Salmo marmoratus) in Slovenia. Molecular Ecology, 11, 2711–2716.

    https://doi.org/10.1046/j.1365-294X.2002.01648.x

    Giménez, L. (2006) Phenotypic links in complex life cycles: Conclusions from studies with decapod crustaceans. In: Integrative and Comparative Biology, 46 (5), 615–622.

    https://doi.org/10.1093/icb/icl010

    Gonzalez, B.C., Martínez, A., Borda, E., Iliffe, T.M., Fontaneto, D. & Worsaae, K. (2017) Genetic Spatial Structure of an anchialine cave annelid indicates connectivity within - but not between - islands of the Great Bahamas Bank. Molecular Phylogenetics and Evolution, 109, 259–270.

    https://doi.org/10.1016/j.ympev.2017.01.003

    Goodman, B.A. & Johnson, P.T.J. (2011) Disease and the extended phenotype: Parasites control host performance and survival through induced changes in body plan. PLoS ONE, 6 (5), e20193.

    https://doi.org/10.1371/journal.pone.0020193

    Google Earth Pro V 7.3.0.3832. (2014) The Bahamas. 24° 38’ 03.18”N, 76° 16’ 52.61”W. DigitalGlobe 2017.

    Hart, C. & Manning, R.B. (1981) The Cavernicolous Caridean Shrimps of Bermuda (Alpheidae, Hippolytidae, and Atyidae). Journal of Crustacean Biology, 1 (3), 441–456.

    https://doi.org/10.2307/1547975

    Hart Jr., C.W., Manning, R.B. & Iliffe, T.M. (1985) The fauna of Atlantic marine caves: evidence of dispersal by sea floor spreading while maintaining ties to deep waters. Proceedings of the Biological Society of Washington, 98 (1), 288–292.

    Hedrick, P.W. & Garcia-Dorado, A. (2016) Understanding Inbreeding Depression, Purging and Genetic Rescue. Trends in Ecology and Evolution, 31 (12), 940–952.

    https://doi.org/10.1016/j.tree.2016.09.005

    Hobbs, H.H., Hobbs, H.H. & Daniel, M.A. (1977) A Review of the Troglobitic Decapod Crustaceans of the Americas. Smithsonian Contributions to Zoology, 244, 1–183.

    https://doi.org/10.5479/si.00810282.244

    Holthuis, L. (1973) Caridean Shrimps Found in Land-locked Saltwater Pools at Four Indo-West Pacific Localities (Sinai Peninsula, Funafuti Atoll, Maui and Hawaii Islands): with the Description of One New Genus and Four New Species. Zoologische Verhandelingen, 128, 3–48.

    Holthuis, L.B. (1963) On Red Coloured Shrimps (Decapoda, Caridea) from Tropical Land-Locked Saltwater Pools. Zoologische mededelingen, 38 (16), 261–179.

    Huelsenbeck, J.P. & Ronquist, F. (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 745–755.

    https://doi.org/10.1093/bioinformatics/17.8.754

    Hunter, R.L., Webb, M.S., Iliffe, T.M. & Bremer, J.R.A. (2008) Phylogeny and historical biogeography of the cave-adapted shrimp genus Typhlatya (Atyidae) in the Caribbean Sea and western Atlantic. Jornal of Biogeography, 35, 65–75.

    Iliffe, T.M. (2000) Anchialine Cave Ecology. In: Wilkens, H., Culver, D.C. & Humphreys, W.F. (Ed.), Ecosystems of the World. 30. Subterranean Ecosystems. Elsevier Science, Amsterdam, pp. 59–76.

    Iliffe, T.M. (2005) Anchialine Caves Biodiversity. In: Culver, D.C. & White, W.B. (Ed.), Encyclopedia of Caves. Elsevier, Burlington, MA, pp. 24–30.

    Iliffe, T.M. & Kornicker, L.S. (2009) Worldwide diving discoveries of living fossil animals from the depths of anchialine and marine caves. Smithsonian Contributions to Marine Sciences, 38, 269–280.

    Ituarte, R.B., Spivak, E.D. & Anger, K. (2007) Intraspecific variability in life-history traits of a “freshwater shrimp”, Palaemonetes argentinus. Annales de Limnologie - International Journal of Limnology, 43 (3), 293–302.

    https://doi.org/10.1051/limn:2007007

    Kano, Y. & Kase, T. (2004) Genetic exchange between anchialine cave populations by means of larval dispersal: The case of a new gastropod species Neritilia cavernicola. Zoologica Scripta, 33 (5), 423–437.

    https://doi.org/10.1111/j.0300-3256.2004.00159.x

    Kappes, H. & Sinsch, U. (2002) Temperature- and predator-induced phenotypic plasticity in Bosmina cornuta and B. pellucida (Crustacea: Cladocera). Freshwater Biology, 47 (10), 1944–1955.

    https://doi.org/10.1046/j.1365-2427.2002.00943.x

    Katoh, K. & Standley, D.M. (2013) MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability. Molecular Biology and Evolution, 30 (4), 772–780.

    https://doi.org/10.1093/molbev/mst010

    Klingenberg, C.P. (2015) Analyzing Fluctuating Asymmetry with Geometric Morphometrics: Concepts, Methods, and Applications. Symmetry, 7, 843–934.

    https://doi.org/10.3390/sym7020843

    Lacy, R.C. & Alaks, G. (2012) Effects of inbreeding on skeletal size and fluctuating asymmetry of Peromyscus polionotus mice. Zoo Biology, 32 (2), 125–133.

    https://doi.org/10.1002/zoo.21035

    Lampert, K.P., Bernal, X.E., Rand, S., Mueller, U.G. & Ryan, M.J. (2007) Island Populations of Physalaemus Pustulosus: History Influences Genetic Diversity and Morphology. Herpetologica, 63 (3), 311–319.

    https://doi.org/10.1655/0018-0831(2007)63[311:IPOPPH]2.0.CO;2

    Lanfear, R., Frandsen, P.B., Wright, A.M., Sendfeld, t. & Calcott, B. (2016) PartitionFinder 2: New Methods for Selecting Paritioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses. Molelcular Biology and Evololution, 34 (3), 772–773.

    https://doi.org/10.1093/molbev/msw260

    Lardies, M.A. & Bozinovic, F. (2008) Genetic Variation for Plasticity in Physiological and Life-History Traits among Populations of an Invasice Species, the terrestrial isopod Porcellio laevis. Evolutionary Ecology Research, 10 (5), 747 –762.

    Laverack, M.S. & Macmillan, D.L. (1999) The sensory dorsal organ of crustaceans: theme and variations. Marine and Freshwater Behaviour and Physiology, 32, 75–86.

    https://doi.org/10.1080/10236249909379040

    Laverack, M.S., Macmillan, D.L., Ritchie, G. & Sandow, S.L. (1996) The Ultrastructure of the Sensory Dorsal Organ of Crustacea. Crustaceana, 69 (5), 636–651.

    https://doi.org/10.1163/156854096X00646

    Lerosey-Aubril, R. & Meyer, R. (2013) The sensory dorsal organs of crustaceans. Biological Reviews, 88 (2), 406–426.

    https://doi.org/10.1111/brv.12011

    Luppi, T.A. & Spivak, E.D. (2007) Morphology of megalopa and first crab of Cyrtographsus angulatus, with comments on the presence of anomalous first crab stage in brachyuran crabs. Journal of Crustacean Biology, 27 (1), 80–89.

    https://doi.org/10.1651/S-2672.1

    Maia S.C.A., Molina W.F. & Maia-Lima F.A. (2009) Analysis of fluctuating asymmetries in marine shrimp Litopenaeus schmitti (Decapoda, Penaaeidae). Pan-American Journal of Aquatic Sciences 4, 55–62.

    Malay, (Machel) D., M.C. & Paulay, G. (2010) Peripatric speciation drives diversification and distributional pattern of reef hermit crabs (Decapoda: Diogenidae: Calcinus). Evolution, 64 (3), 634–662.

    https://doi.org/10.1111/j.1558-5646.2009.00848.x

    Manning, R.B. & Hart, C.W. (1984) The status of the hippolytid shrimp genera Barbouria and Ligur (Crustacea: Decapoda): A Reevaluation. Proceedings of the Biological Society of Washington, 97, 655–665.

    Martens, E., von (1872) Über cubanische Crustaceen nach den Sammlungen Dr. J. Gundlach’s. Archiv für Naturgeschichte, 38 (1), 77–147, Plates 4–5.

    McInerney, C.E., Maurice, L., Robertson, A.L., Knight, L.R.F.D., Arnscheidt, J., Venditti, C., Dooley, J.S.G., Mathers, T., Matthijs, S., Eriksson, K., Proudlove, G.S. & Hänfling, B. (2014) The ancient Britons: Groundwater fauna survived extreme climate change over tens of millions of years across NW Europe. Molecular Ecology, 23 (5), 1153–1166.

    https://doi.org/10.1111/mec.12664

    Mejía, L.M., Zarza, E. & López, M. (2008) Barbouria yanezi sp. nov., a new species of cave shrimp (Decapoda, Barbouriidae) from Cozumel Island, Mexico. Crustaceana, 81 (6), 663–672.

    https://doi.org/10.1163/156854008784513474

    Moncada, F.G., & Gomes, O. (1980) Alguenos aspectos biológicos de três especies del gênero Callinectes (Crustacea, Decapoda). Revista Cubana de Investigación Pequera, 5, 1–35.

    Munasinghe, D.H.N. & Senevirathna J.D.M. (2015) Phenotypic plasticity and genetic variation of two wild populations of green tiger shrimp (Penaeus semisulcatus–De Haan, 1844). International Journal of Marine Science, 5 (5), 1–8.

    https://doi.org/10.5376/ijms.2015.05.0005

    Nishizaki, M.T., Barron, S. & Carew, E. (2015) Thermal stress increases fluctuating asymmetry in marine mussels: environmental variation and developmental instability. Ecosphere, 6 (5), 85.

    https://doi.org/10.1890/ES14-00399.1

    O’Grady, J.J., Brook, B.W., Reed, D.H., Ballou, J.D., Tonkyn, D.W. & Frankham, R. (2006) Realistic levels of inbreeding depression strongly affect extinction risk in wild populations. Biological Conservation, 133 (1), 42–51.

    https://doi.org/10.1016/j.biocon.2006.05.016

    Oha, T. & Paal, J. (2004) Multivariate analysis of morphological variation among closely related species Bromus Japonicus, B. squarrosus and B. arvensis (Paceae) in comparison with isozyme evidence. Nordic Journal of Botany, 24 (6), 691–702.

    https://doi.org/10.1111/j.1756-1051.2004.tb01939.x

    Onaga, H., Fiedler, G. & Baeza, J. (2012) Protandric simultaneous hermaphroditism in Parhippolyte misticia (Clark, 1989)(Caridea: Hippolytidae): implications for the evolution of mixed sexual systems in. Journal of Crustacean Biology, 32 (3), 383–394.

    https://doi.org/10.1163/193724012X626520

    Palumbi, S., Martin, A., Romano, S., McMillan, W.O., Stice, L. & Grabowski, G. (1991) The Simple Fool’s Guide to PCR. Department of Zoology and Kewalo Marine Laboratory, University of Hawaii, Honolulu, 44 pp.

    Pérez-Moreno, J.L., Iliffe, T.M. & Bracken-Grissom, H.D. (2016) Life in the Underworld: Anchialine cave biology in the era of speleogenomics. International Journal of Speleology, 45 (2), 149–170.

    https://doi.org/10.5038/1827-806X.45.2.1954

    Perry, W.L., Feder, J.L & Lodge, D.M. (2001) Implications of Hydridization between Introducted and Resident Orconectes Crayfishes. Conservation Biology, 15 (6), 1656–1666.

    https://doi.org/10.1046/j.1523-1739.2001.00019.x

    Porter, M.L., Perez-Losada, M. & Crandall, K.A. (2005) Model-based multi-locus estimation of decapod phylogeny and divergence times. Molecular Phylogenetics and Evolution, 37, 355–369.

    https://doi.org/10.1016/j.ympev.2005.06.021

    Page, T.J., Short, J.W., Humphrey, C.L., Hillyer, M.J. & Hughes, J.M. (2008) Molecular systematics of the Kakaducarididae (Crustacea: Decapoda: Caridea). Molecular Phylogenetics and Evolution, 46, 1003–1014.

    https://doi.org/10.1016/j.ympev.2007.12.020

    R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, Available from: https://www.R-project.org/

    Rafineque, C.S. (1815) Analyse de la Nature, ou Tableau de l’Univers et de Corps Organisés. Palermo, L’Imprimerie de Jean Barravecchia. 224 pp.

    https://doi.org/10.5962/bhl.title.106607

    Rathbun, M.J. (1912) Some Cuban Crustacea, with notes on the Astacidae by Walter Faxon, and a list of Isopoda, by Harriet Richardson. Bulletin of the Museum of Comparative Zoology, 54 (15), 451–460, Pls. 1–5.

    Reuschel, S. & Schubart, C.D. (2007) Contrasting genetic diversity with phenotypic diversity in coloration and size in Xantho poressa (Brachyura: Xanthidae), with new results on its ecology. Marine Ecology, 28 (2), 296–305.

    https://doi.org/10.1111/j.1439-0485.2006.00139.x

    Ribardière, A., Daguin-Thiébaut, C., Houbin, C., Coudret, J., Broudin, C., Timsit, O. & Broquet, T. (2017) Geographically distinct patterns of reproductive isolation and hybridization in two sympatric species of the Jaera albifrons complex (marine isopods). Ecology and Evolution, 7 (14), 5352–5365.

    https://doi.org/10.1002/ece3.3106

    Ripley, B., Venables, B., Bates, D.M., Hornik, K., Gebhardt, A. & Firth, D. (2018) Support Functions and Datasets for Venables and Ripley’s MASS. Available from: http://www.stats.ox.ac.uk/pub/MASS4/

    Roberts, D.W. (2016) Ordination and Multivariate Analysis for Ecology. Available from: http://ecology.msu.montana.edu/labdsv/R

    Robles, R., Schubart, C.D., Conde, J.E., Carmona-Suarez, C., Alvarez, F., Villalobos, J.L. & Felder, D.L. (2007) Molecular phylogeny of the American Callinectes Stimpson, 1860 (Brachyura: Portunidae), based on two partial mitochondrial genes. Marine Biology, 150, 1265–1274.

    https://doi.org/10.1007/s00227-006-0437-7

    Russ, A., Santos, S.R. & Muir, C. (2010) Genetic population structure of an anchialine shrimp, Metabetaues lohena (Crustacea: Alpheidae), in the Hawaiin Islands. Revista de Biología Tropical, 58 (1), 159–170.

    https://doi.org/10.15517/rbt.v58i1.5201

    Santos, S.R. (2006) Patterns of genetic connectivity among anchialine habitats: a case study of the endemic Hawaiin shrimp Halocaridina rubra on the island of Hawaii. Molecular Ecology, 15, 2699–2718.

    https://doi.org/10.1111/j.1365-294X.2006.02965.x

    Sket, B. (2005) Anchialine Caves. In: Culver, D.C. & White, W.B. (Eds.), Encyclopedia of Caves. Elsevier Academic Press, 30–37.

    Smith, L.D. & Palmer, A.R. (1994) Effects of manipulated diet on size and performance of brachyuran crab claws. Science, 264 (5159), 710–712.

    https://doi.org/10.1126/science.264.5159.710

    Song, H., Buhay, J.E., Whiting, M.F. & Crandall, K.A. (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. PNAS, 105 (36), 13486–13491.

    https://doi.org/10.1073/pnas.0803076105

    Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analyses of large phylogenies. Bioinformatics, 30 (9), 1312-1313.

    https://doi.org/10.1093/bioinformatics/btu033

    Stearns, S. (1989) The evolutionary significance of phenotypic plasticity. BioScience, 39 (7), 436–445.

    https://doi.org/10.2307/1311135

    Steinauer, M.L., Nickol, B.B. & Ortí, G. (2007) Cryptic speciation and patterns of phenotypic variation of a highly variable acanthocephalan parasite. Molecular Ecology, 16 (19), 4097–4109.

    https://doi.org/10.1111/j.1365-294X.2007.03462.x

    Stibor, H. & Lüning, J. (1994) Predator-inudced phenotypic variation in the pattern of growth and reproduction in Daphnia hyalina (Crustacea: Cladocera). British Ecological Society, 8 (1), 97–101.

    https://doi.org/10.2307/2390117

    Stock, J.H. (1986) The concept “anchialine” reconsidered. Stygologia, 2, 90–92.

    Swofford, D.L. (2002) PAUP*: phylogenetic analysis using parsimony (* and other methods). Sinauer Associates, Sunderland, MA.

    Trussell, G.C. (1996) Phenotypic plasticity in an intertidal snail: The role of a common crab predator. Evolution, 50 (1), 448–454.

    https://doi.org/10.1111/j.1558-5646.1996.tb04507.x

    Trussell, G.C. & Smith, L.D. (2000) Induced defenses in response to an invading crab predator: An explanation of historical and geographic phenotypic change. PNAS, 97 (5), 2123–2127.

    https://doi.org/10.1073/pnas.040423397

    Tsang, L.M., Ma, K.Y., Ahyong, S.T., Chan, T.-Y. & Chu, K.H. (2008) Phylogeny of Decapoda using two nuclear protein-coding genes: origin and evolution of the Reptantia. Molelcuar Phylogenetics and Evolution, 48, 359–368.

    https://doi.org/10.1016/j.ympev.2008.04.009

    Vogt, G., Huber, M., Thiemann, M., van den Boogaart, G., Schmitz, O.J. & Schubart, C.D. (2008) Production of different phenotypes from the same genotype in the same environment by developmental variation. The Journal of Experimental Biology, 211 (4), 510–23.

    https://doi.org/10.1242/jeb.008755

    Weese, D.A., Fujita, Y. & Santos, S.R. (2013) Multiple colonizations lead to cryptic biodiversity in an island ecosystem: comparative phylogeography of anchialine shrimp species in the Ryukyu Archipelago, Japan. Biological Bulletin, 225, 24–41.

    https://doi.org/10.1086/BBLv225n1p24

    Weese, D.A., Fujita, Y., Hidaka, M. & Santos, S.R. (2012) The Long and Short of it: Genetic Variation and Population Structure of the Anchialine Atyid Shrimp Caridina rubella on Miyako-Jima, Japan. Journal of Crustacean Biology, 32 (1), 109–117.

    https://doi.org/10.1163/193724011X615389

    Wicksten, M.K. (1996) Parhippolye cavernicola, new species (Decapoda: Caridea: Hippolytidae) from the Tropical Eastern Pacific, with taxonomic remarks on the genera Somersiella and Koror. Journal of Crustacean Biology, 16 (1), 201–207.

    https://doi.org/10.2307/1548941

    Wolf, H.G. & Mort, M.A. (1986) Inter-specific hybridization underlies phenotypic varaibility in Daphnai populations. Oecologia, 68, 507–511.

    https://doi.org/10.1007/BF00378763