Skip to main content
Log in

Incongruence between molecular and morphological characters in the southern king crabs Lithodes santolla and Lithodes confundens (Decapoda: Anomura)

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

The use of genetic tools has a relevant role in fishery resource management and conservation, for example, when used in species delimitation. Morphological variation can occur as an adaptative or plastic response to environmental variation, and therefore, be mistakenly used as a criterion to delimit species. Particularly, Lithodes santolla and Lihodes confundens, two commercially important lithodid species from sub-Antarctic South America, are mainly differentiated by the number and size of spines on the carapace and pereiopods. However, variability in the size of spines of L. santolla has been reported. We evaluated whether these two morphospecies constitute reciprocally monophyletic clades at the molecular level using mitochondrial markers, and performed a detailed morphological analysis of the carapace to search for correspondence between genetic and morphological differences. The Bayesian phylogenetic reconstruction showed that L. santolla and L. confundens belong to two sister clades. However, individuals identified as L. santolla and L. confundens did not resolve as reciprocally monophyletic groups. Instead, one clade was formed by individuals belonging to both morphospecies and was widely distributed, while the other one was exclusively formed by L. santolla, and its members were only found near Puerto Montt and in the Beagle Channel. No morphological characters were found on the carapace that could differentiate individuals belonging to each genetic clade. Either if the two genetic clades constitute species or remnants of two species that are merging through introgression, they represent two evolutionary significant lineages, and measures should be taken to preserve both. Our study suggests the need to revise the use of the number of spines as a relevant taxonomic character in the taxonomy of Lithodes, and to implement molecular genetic methods to control fisheries.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Addison JA, Hart MW (2005) Colonization, dispersal, and hybridization influence phylogeography of North Atlantic sea urchins (Strongylocentrotus droebachiensis). Evol 59:532–543

    CAS  Google Scholar 

  • Ahyong ST, Chan TY (2010) Lithodes formosae, a new species of king crab from Taiwan (Crustacea: Decapoda: Lithodidae). Zootaxa 2332:61–68

    Google Scholar 

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622

    Article  Google Scholar 

  • Anosov SE, Spiridonov VA, Neretina TV, Uryupova EF, Schepetov D (2015) King crabs of the western Atlantic sector of Antarctic and adjacent areas: new records, molecular barcode data and distribution (Crustacea: Decapoda: Lithodidae). Polar Biol 38:231–249

    Article  Google Scholar 

  • Avise JC, Saunders NC (1984) Hybridization and introgression among species of sunfish (Lepomis): Analysis by mitochondrial DNA and allozyme markers. Genet 108:237–255

    CAS  Google Scholar 

  • Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Bernatchez L, Glémet H, Wilson CC, Danzmann RG (1995) lntrogression and fixation of Arctic char (Salvelinus alpinus) mitochondrial genome in an allopatric population of brook trout (Salvelinus fontinalis). Can J Fish Aquat Sci 52:179–185

    Article  CAS  Google Scholar 

  • Boschi EE, Gavio MA (2005) On the distribution of decapod crustaceans from the Magellan Biogeographic Province and the Antarctic region. Sci Mar 69:195–200

  • Camargo A, Sites JJ (2013) Species delimitation: a decade after the renaissance. In: Pavlinov IY (ed) The species problem—ongoing issues, Intech, pp 225–247

  • Cavallotto JL, Violante RA, Hernández-Molina FJ (2011) Geological aspects and evolution of the Patagonian continental margin. Biol J Linn Soc 103:346–362

    Article  Google Scholar 

  • Ceballos SG, Lessa EP, Victorio MF, Fernández DA (2012) Phylogeography of the sub-Antarctic notothenioid fish Eleginops maclovinus: evidence of population expansion. Mar Biol 159:499–505

    Article  Google Scholar 

  • Darling JA (2011) Interspecific Hybridization and Mitochondrial Introgression in Invasive Carcinus Shore Crabs. PLoS ONE 6:e17828

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Davis JLD, Eckert-Mills MG, Young-Williams AC, Hines AH, Zohar Y (2005) Morphological conditioning of a hatchery-raised invertebrate, Callinectes sapidus, to improve field survivorship after release. Aquac 243:147–158

    Article  Google Scholar 

  • Dawson EW, Yaldwyn JC (1985) King crabs of the world or the world of king crabs: an overview of identity and distribution–with illustrated diagnostic keys to the genera of the Lithodidae and to the species of Lithodes. In: Melteff BR (ed) Proceedings of the International King Crab Symposium. Alaska Sea Grant Report No. 85–12, University of Alaska, Anchorage, pp 69–106

  • Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2013) ‘InfoStat versión 2013.’ Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar

  • Drummond AJ, Ho SYW, Phillips MJ, Rambaut A (2006) Relaxed phylogenetics and dating with confidence. PLoS Biol 4:e88

    Article  PubMed Central  PubMed  Google Scholar 

  • Drummond AJ, Suchard MA, Xie D, Rambaut A (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29:1969–1973

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among haplotypes: applications to human mitochondrial DNA restriction data. Genet 136:479–491

    Google Scholar 

  • Folmer M, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial Cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Fu Y-X (1997) Statistical test of neutrality of mutations against population growth, hitchhiking and background selection. Genet 147:915–925

    CAS  Google Scholar 

  • Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423

    Article  Google Scholar 

  • Goloboff PA, Farris JS, Nixon K (2003) ‘TNT: tree analysis using new technology, version 1.1.’ http://www.zmuc.dk/public/phylogeny

  • Goloboff PA, Farris JS, Nixon KC (2008) TNT, a free program for phylogenetic analysis. Cladistics 24:774–786

    Article  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hall S (2010) The evolutionary history and phylogeny of the Lithodinae (Decapoda: Anomura: Lithodidae). Dissertation, University of Southampton

  • Hall S, Thatje S (2011) Temperature-driven biogeography of the deep-sea family Lithodidae (Crustacea: Decapoda: Anomura) in the Southern Ocean. Polar Biol 34:363–370

    Article  Google Scholar 

  • Harper FM, Hart MW (2007) Morphological and phylogenetic evidence for hybridization and introgression in a sea star secondary contact zone. Invertebr Biol 126:373–384

    Article  Google Scholar 

  • Harris LN, Howland KL, Kowalchuk MW, Bajno R, Lindsay MM, Taylor EB (2013) Microsatellite and mtDNA analysis of lake trout, Salvelinus namaycush, from Great Bear Lake, Northwest Territories: impacts of historical and contemporary evolutionary forces on Arctic ecosystems. Ecol Evol 3:145–161

    Article  PubMed Central  Google Scholar 

  • Hasegawa M, Kishino K, Yano T (1985) Dating the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    Article  CAS  PubMed  Google Scholar 

  • Holsinger K (2012) Tajima’s D, Fu’s Fs, Fay and Wu’s H, and Zeng et al.’s E. In: Holsinger K (ed) Lecture notes in population genetics, pp 239–244

  • Kimura M (1981) Estimation of evolutionary distances between homologous nucleotide sequences. Proc Natl Acad Sci USA 78:454–458

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ladner JT, Palumbi SR (2012) Extensive sympatry, cryptic diversity and introgression throughout the geographic distribution of two coral species complexes. Mol Ecol 21:2224–2238

    Article  PubMed  Google Scholar 

  • Lessios HA, Pearse JS (1996) Hybridization and introgression between Indo-Pacific species of Diadema. Mar Biol 126:715–723

    Article  Google Scholar 

  • Lezcano AH, González-José R, Spivak ED, Dellatorre FG (2012) Geographic differences in the carapace shape of the crab Cyrtograpsus affinis (Decapoda: Varunidae) and its taxonomic implications. Sci Mar 76:329–337

  • Lovrich GA, Tapella F (2014) Southern King Crabs. In: Stevens BG (ed) King crabs of the world: biology and fisheries management. CRC Press, Boca Raton, pp 441–476

    Google Scholar 

  • Lovrich GA, Perroni M, Vinuesa JH, Tapella F, Chizzini AC, Romero MC (2002) Occurrence of Lithodes confundens (Decapoda: Anomura) in the intertidal of the Southwestern Atlantic. J Crustac Biol 22:894–902

    Article  Google Scholar 

  • Macpherson E (1988) Revision of the family Lithodidae Samouelle, 1819 (Crustacea, Decapoda, Anomura) in the Atlantic Ocean. Monografías de Zoología Marina 2:9–153

    Google Scholar 

  • McLaughlin PA (2014) Systematics of king crabs. In: Stevens BG (ed) King crabs of the world: biology and fisheries management. CRC Press, Boca Raton, pp 31–46

    Chapter  Google Scholar 

  • Nordborg N (2007) Coalescent theory. In: Balding DJ, Bishop M, Cannings C (eds) Handbook of statistical genetics. Wiley, New Jersey, pp 843–877

  • Ocampo EH, Robles R, Terossi M, Nuñez JD, Cledón M, Mantelatto F (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

    Article  Google Scholar 

  • Otto R (2014) History of king crab fisheries with special reference to the North Pacific Ocean: development, maturity and senescence. In: Stevens BG (ed) King crabs of the world: biology and fisheries management. CRC Press, Boca Raton, pp 81–138

    Chapter  Google Scholar 

  • Palero F, Hall S, Clark PF, Johnston D, Mackenzie-Dodds J, Thatje S (2010) DNA extraction from formalin-fixed tissue: new light from the deep sea. Sci Mar 74:465–470

  • Pastorini J, Zaramody A, Curtis DJ, Nievergelt CM, Mundy NI (2009) Genetic analysis of hybridization and introgression between wild mongoose and brown lemurs. BMC Evol Biol 9:32

    Article  PubMed Central  PubMed  Google Scholar 

  • Pérez-Barros P, Tapella F, Romero MC, Calcagno J, Lovrich G (2004) Benthic decapod crustaceans associated with captures of Munida spp. (Decapoda: Anomura) in the Beagle Channel, Argentina. Sci Mar 68:237–246

  • Pérez-Barros P, D’Amato ME, Guzmán NV, Lovrich GA (2008) Taxonomic status of two South American sympatric squat lobsters, Munida gregaria and M. subrugosa (Crustacea: Decapoda: Galatheidae), challenged by DNA sequence information. Biol J Linn Soc 94:421–434

    Article  Google Scholar 

  • Pérez-Barros P, Calcagno J, Lovrich G (2011) Absence of a prezygotic behavioural barrier to gene flow between the two sympatric morphs of the squat lobster Munida gregaria (Fabricius, 1793) (Decapoda: Anomura: Galatheidae). Helgol Mar Res 65:513–523

    Article  Google Scholar 

  • Pérez-Barros P, Lovrich GA, Calcagno JA, Confalonieri VA (2014) Is Munida gregaria (Crustacea: Decapoda: Munididae) a truly transpacific species? Polar Biol 37:1413–1420

    Article  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

  • Rabassa J, Coronato A, Martínez O (2011) Late Cenozoic glaciations in Patagonia and Tierra del Fuego: an updated review. Biol J Linn Soc 103:316–335

    Article  Google Scholar 

  • Rambaut A, Drummond AJ (2003) Tracer (computer program). http://tree.bio.ed.ac.uk/software/tracer/

  • Reiss RA, Schwert DP, Ashworth AC (1995) Field preservation of Coleoptera for molecular genetics analyses. Environ Entomol 24:716–719

    Article  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinform 19:1572–1574

    Article  CAS  Google Scholar 

  • Schneider S, Excoffier L (1999) Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genet 152:1079–1089

    CAS  Google Scholar 

  • Schubart CD, Diesel R, Hedges SB (1998) Rapid evolution to terrestrial life in Jamaican crabs. Nature 393:363–365

    Article  CAS  Google Scholar 

  • Schubart CD, Neigel JE, Felder DL (2000) Use of the mitochondrial 16S rRNA gene for phylogenetic and population studies of Crustacea. Crustac Issues 12:817–830

    Google Scholar 

  • Schubart CD, Conde JE, Carmona-Suárez C, Robles R, Felder DL (2001) Lack of divergence between 16S mtDNA sequences of the swimming crabs Callinectes bocourti and C. maracaiboensis (Brachyura: Portunidae) from Venezuela. Fish Bull 99:475–481

    Google Scholar 

  • Sotelano MP, Gowland-Sainz MF, Diez MJ, Lovrich GA (2013) Distribution of Lithodes confundens Macpherson, 1988 (Decapoda, Anomura) along the Atlantic continental shelf of southern South America. Crustac 86:246–252

    Article  Google Scholar 

  • Sotelo G, Morán P, Posada D (2009) Molecular phylogeny and biogeographic history of the European Maja spider crabs (Decapoda, Majidae). Mol Phylogenet Evol 53:314–319

    Article  CAS  PubMed  Google Scholar 

  • Spivak ED, Schubart CD (2003) Species status in question: a morphometric and molecular comparison of Cyrtograpsus affinis and C. altimanus (Decapoda, Brachyura, Varunidae). J Crustac Biol 23:212–222

    Article  Google Scholar 

  • Stillman JH, Reeb CA (2001) Molecular phylogeny of eastern Pacific porcelain crabs, genera Petrolisthes and Pachycheles, based on the mtDNA 16S rDNA sequence: phylogeographic and systematic implications. Mol Phylogenet Evol 19:236–245

    Article  CAS  PubMed  Google Scholar 

  • Tajima F (1989a) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genet 123:585–595

    CAS  Google Scholar 

  • Tajima F (1989b) The effect of change in population size on DNA polymorphism. Genet 123:597–601

    CAS  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tavaré S (1986) Some probabilistic and statistical problems in the analysis of DNA sequences. In: Miura RM (ed) Some mathematical questions in biology—DNA sequence analysis, American Mathematical Society, Providence (RI) pp 57–86

  • Vinuesa JH (1985) Differential aspects of the southern king crab (Lithodes antarcticus) in two latitudinally separated locations. In: Melteff B (ed) Proceedings of the international King Crab symposium, Alaska Sea Grant Report 85-12, University of Alaska, pp 267–279

  • Westphal MJ, Eckert GL, Tamone SL (2014) Comparison of first year growth among field, hatchery- and laboratory-raised juvenile red king crab, Paralithodes camtschaticus (Tilesius, 1815), in Alaska. J Crustac Biol 34:319–325

    Article  Google Scholar 

  • Zaklan SD (2002) Review of the family Lithodidae (Crustacea: Anomura: Paguroidea): distribution, biology, and fisheries. In: Paul AJ, Dawe G, Elner RW, Jamieson G, Kruse GH, Otto RS, Sainte-Marie B, Shirley TC, Woodby D (eds) Crabs in cold water regions: biology, management, and economics. Sea Grant College Program, University of Alaska, pp 751–845

Download references

Acknowledgments

We greatly appreciate the help of crews and captains of the RV Puerto Deseado. María Gowland-Sainz, Olga Florentín and Marcelo Pérez helped us with sampling and Anabela Petraroia helped us with lab work. The comments of three anonymous reviewers greatly improved this manuscript. This study was funded by a grant of the Argentine Agencia Nacional de Promoción Científica y Tecnológica, Fondo para la Investigación Científica y Tecnológica, Préstamo BID—PICT 2010-2529, CONICET, Universidad Maimónides and Fundación de Historia Natural Félix de Azara.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia Pérez-Barros.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 100 kb)

Supplementary material 2 (PDF 89 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pérez-Barros, P., Confalonieri, V.A., Paschke, K. et al. Incongruence between molecular and morphological characters in the southern king crabs Lithodes santolla and Lithodes confundens (Decapoda: Anomura). Polar Biol 38, 2097–2107 (2015). https://doi.org/10.1007/s00300-015-1770-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-015-1770-4

Keywords

Navigation