Skip to main content

Advertisement

Log in

Cryptic species of cardinalfish with evidence for old and new divergence

  • Report
  • Published:
Coral Reefs Aims and scope Submit manuscript

Abstract

Larval dispersal and limited knowledge of physical boundaries challenge our understanding of the processes that drive genetic divergence and potential speciation in the marine environment. Divergence, both within and between populations of marine taxa, is not uncommon, but spatial and temporal stability of observed genetic structure is not well known. Previously, we detected large genetic differences among populations of the cardinalfish species Ostorhinchus doederleini inhabiting adjacent coral reefs. Here, we determined the spatial and temporal persistence of these genetic structures over the course of ten consecutive generations. Using microsatellite markers, we detected large changes (genetic population distance, D est, ranged from 0.04 to 0.46) in the genetic structure in some years, but some reefs maintained the same populations for nearly all sampling years. As this species’ life span does not exceed 1 yr, persistence of distinct reef populations suggests natal homing. Mitochondrial identity based on two mtDNA markers corroborates the nuclear genetic evidence for genetic differences large enough to constitute different clades and even cryptic species in O. doederleini, which, based on gross morphology, was thought to be a single taxon. Habitat specialization was observed in one clade that exclusively inhabited reef lagoons, while all clades could be observed on reef slopes. We suggest that local habitat recognition combined with local population recognition and selection against hybrids can form barriers that maintain a cryptic species complex.

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

References

  • Allen GR (2009) Field guide to marine fishes of tropical Australia and Southeast Asia. Western Australian Museum, Perth

    Google Scholar 

  • Atema J, Kingsford M, Gerlach G (2002) Larval reef fish could use odour for detection, retention and orientation to reefs. Mar Ecol Prog Ser 241:151–160

    Article  Google Scholar 

  • Baldwin CC, Mounts JH, Smith DG, Weigt LA (2009) Genetic identification and color descriptions of early life-history stages of Belizean Phaeoptyx and Astrapogon (Teleostei: Apogonidae) with comments on identification of adult Phaeoptyx. Zootaxa 2008:1–22

    Google Scholar 

  • Bargelloni L, Alarcon JA, Alvarez MC, Penzo E, Magoulas A, Reis C, Patarnello T (2003) Discord in the family Sparidae (Teleostei): divergent phylogeographical patterns across the Atlantic-Mediterranean divide. J Evol Biol 16:1149–1158

    Article  CAS  PubMed  Google Scholar 

  • Bay LK, Jones GP, McCormick MI (2001) Habitat selection and aggression as determinants of spatial segregation among damselfish on a coral reef. Coral Reefs 20:289–298

    Article  Google Scholar 

  • Belkhir K, Borsa P, Goudet J, Chikhi L, Bonhomme F (1997) Genetix v. 3.0, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome et Populations, CNRS UPR 9060, Université Montpellier 2, Montpellier

  • Bernardi G, Vagelli A (2004) Population structure in Banggai cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Mar Biol 145:803–810

    Google Scholar 

  • Bickford D, Lohman DJ, Sodhi NS, Ng PKL, Meier R, Winker K, Ingram KK, Das I (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155

    Article  PubMed  Google Scholar 

  • Burford MO, Bernardi G, Carr MH (2011) Analysis of individual year-classes of a marine fish reveals little evidence of first-generation hybrids between cryptic species in sympatric regions. Mar Biol 158:1815–1827

    Article  Google Scholar 

  • Christie MR, Johnson DW, Stallings CD, Hixon MA (2010) Self-recruitment and sweepstakes reproduction amid extensive gene flow in a coral-reef fish. Mol Ecol 19:1042–1057

    Article  PubMed  Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol Notes 9:1657–1660

    Article  CAS  Google Scholar 

  • Colborn J, Crabtree RE, Shaklee JB, Pfeiler E, Bowen BW (2001) The evolutionary enigma of bonefishes (Albula spp.): cryptic species and ancient separations in a globally distributed shorefish. Evolution 55:807–820

    Article  CAS  PubMed  Google Scholar 

  • Døving KB, Stabell OB, Östlund-Nilsson S, Fisher R (2006) Site fidelity and homing in tropical coral reef cardinalfish: are they using olfactory cues? Chem Senses 31:265–272

    Article  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32:1792–1797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620

    Article  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 Res 10:564–567

    Article  Google Scholar 

  • Farnsworth CA, Bellwood DR, van Herwerden L (2010) Genetic structure across the GBR: evidence from short-lived gobies. Mar Biol 157:945–953

    Article  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Finn MD, Kingsford MJ (1996) Two-phase recruitment of apogonids (Pisces) on the Great Barrier Reef. Mar Freshw Res 47:423–432

    Article  Google Scholar 

  • Fisher R (2005) Swimming speeds of larval coral reef fishes: impacts on self-recruitment and dispersal. Mar Ecol Prog Ser 285:223–232

    Article  Google Scholar 

  • Gerlach G, Hodgins-Davis A, Avolio C, Schunter C (2008) Kin recognition in zebrafish: a 24-hour window for olfactory imprinting. Proc R Soc Lond B Biol Sci 275:2165–2170

    Article  Google Scholar 

  • Gerlach G, Atema J, Kingsford MJ, Black KP, Miller-Sims V (2007) Smelling home can prevent dispersal of reef fish larvae. Proc Natl Acad Sci USA 104:858–863

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gerlach G, Jüterbock A, Krämer P, Deppermann J, Harmand P (2010) Calculations of population differentiation based on GST and D: forget GST but not the statistics! Mol Ecol 19:3845–3852

    Article  PubMed  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:1–9

    Google Scholar 

  • Heads M (2005) Towards a panbiogeography of the seas. Biol J Linn Soc Lond 84:675–723

    Article  Google Scholar 

  • Hedgecock D (1994) Temporal and spatial genetic structure of marine animal populations in the California current. California Cooperative Oceanic Fisheries Investigations Reports 35:73–81

    Google Scholar 

  • Hickey RA, Clements KD (2005) Genome size evolution in New Zealand triplefin fishes. J Hered 96:356–362

    Article  CAS  PubMed  Google Scholar 

  • Hinz C, Gebhardt K, Hartmann AK, Sigman L, Gerlach G (2012) Influence of kinship and MHC class II genotype on visual traits in zebrafish larvae (Danio rerio). PLoS One 7(e5118210):5118137

    Google Scholar 

  • Hinz C, Kobbenbring S, Kress S, Sigman L, Müller A, Gerlach G (2013a) Kin recognition in zebrafish, Danio rerio, is based on imprinting on olfactory and visual stimuli. Anim Behav 85:925–930

    Article  Google Scholar 

  • Hinz C, Namekawa I, Behrmann-Godel J, Oppelt C, Jaeschke A, Müller A, Friedrich RW, Gerlach G (2013b) Olfactory imprinting is triggered by MHC peptide ligands. Sci Rep 3:2800

    Article  PubMed  PubMed Central  Google Scholar 

  • Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026

    Article  PubMed  Google Scholar 

  • Kingsford MJ, Finn MD, O’Callaghan MD, Atema J, Gerlach G (2014) Planktonic larval duration, age and growth of Ostorhinchuns doederleini (Pisces: Apogonidae) on the southern Great Barrier Reef, Australia. Mar Biol 161:245–259

    Article  Google Scholar 

  • Kingsford MJ, Leis JM, Shanks A, Lindeman KC, Morgan SG, Pineda J (2002) Sensory environments, larval abilities and local self-recruitment. Bull Mar Sci 70:309–340

    Google Scholar 

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216

    Article  Google Scholar 

  • Larson RJ, Julian RM (1999) Spatial and temporal genetic patchiness in marine populations and their implications for fisheries management. California Cooperative Oceanic Fisheries Investigations Reports 40:94–99

    Google Scholar 

  • Lee WJ, Conroy J, Howell WH, Kocher TD (1995) Structure and evolution of teleost mitochondrial control regions. J Mol Evol 41:54–66

    Article  CAS  PubMed  Google Scholar 

  • Leis JM, Siebeck U, Dixson DL (2011) How nemo finds home: the neuroecology of dispersal and of population connectivity in larvae of marine fishes. Integr Comp Biol 51:826–843

    Article  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphic data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Liu SYV, Dai CF, Allen GR, Erdmann MV (2012) Phylogeography of the neon damselfish Pomacentrus coelestis indicates a cryptic species and different species origins in the west Pacific Ocean. Mar Ecol Prog Ser 458:155–167

    Article  Google Scholar 

  • Mabuchi K, Okuda N, Kokita T, Nishida M (2003) Genetic comparison of two color-morphs of Apogon properuptus from southern Japan. Ichthyol Res 50:293–296

    Article  Google Scholar 

  • Mabuchi K, Fraser TH, Song H, Azuma Y, Nishida M (2014) Revision of the systematics of the cardinalfishes (Percomorpha: Apogonidae) based on molecular analyses and comparative reevaluation of morphological characters. Zootaxa 3846:151–203

    Article  PubMed  Google Scholar 

  • McMillan WO, Palumbi SR (1997) Rapid rate of control-region evolution in pacific butterflyfishes (Chaetodontidae). J Mol Evol 45:473–484

    Article  CAS  PubMed  Google Scholar 

  • Miller-Sims V, Atema J, Kingsford MJ, Gerlach G (2004) Characterization and isolation of DNA microsatellite primers in the cardinalfish (Apogon doederleini). Mol Ecol Notes 4:336–338

    Article  CAS  Google Scholar 

  • Miller-Sims V, Gerlach G, Kingsford MJ, Atema J (2011) Reef odour imprinting: coral reef fish demonstrate stable olfactory preference for their settlement reef. Mar Freshwr Behav Physiol 44:133–141

    Article  Google Scholar 

  • Mirams AGK, Treml EA, Shields JL, Liggins L, Riginos C (2011) Vicariance and dispersal across an intermittent barrier: population genetic structure of marine animals across the Torres Strait land bridge. Coral Reefs 30:937–949

    Article  Google Scholar 

  • Mouritsen H, Atema J, Kingsford MJ, Gerlach G (2013) Sun compass orientation helps coral reef fish larvae return to their natal reef. PLoS One 8:e66039

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Neilson ME, Stepien CA (2009) Evolution and phylogeography of the tubenose goby genus Proterorhinus (Gobiidae: Teleostei): evidence for new cryptic species. Biol J Linn Soc Lond 96:664–684

    Article  Google Scholar 

  • Nosil P (2012) Ecological speciation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Palumbi SR, Grabowsky G, Duda T, Geyer L, Tachino N (1997) Speciation and population genetic structure in tropical Pacific sea urchins. Evolution 51:1506–1517

    Article  Google Scholar 

  • Pandolfi JM, Kelley R (2008) The Great Barrier Reef in time and space: geology and palaeobiology. In: Hutchings P, Kingsford MJ, Hoegh-Guldberg O (eds) The Great Barrier Reef: biology, environment and management. Springer, Dordrecht, The Netherlands, pp 17–28

    Google Scholar 

  • Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420

    Article  CAS  PubMed  Google Scholar 

  • Paxton JR, Hoese DF, Allen GR, Hanley JE (1989) Pisces. Australian Government Publishing Service, Canberra, Petromyzontidae to Carangidae

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pritchard J, Falush D, Stephens M (2002) Inference of population structure in recently admixed populations. Am J Hum Genet 71:177

    Google Scholar 

  • Radford CA, Stanley JA, Simpson SD, Jeffs AG (2011) Juvenile coral reef fish use sound to locate habitats. Coral Reefs 30:295–305

    Article  Google Scholar 

  • Rocha LA, Bowen BW (2008) Speciation in coral-reef fishes. J Fish Biol 72:1101–1121

    Article  Google Scholar 

  • Rocha LA, Lindeman KC, Rocha CR, Lessios HA (2008) Historical biogeography and speciation in the reef fish genus Haemulon (Teleostei: Haemulidae). Mol Phylogenet Evol 48:918–928

    Article  CAS  PubMed  Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    CAS  PubMed  Google Scholar 

  • Rueger T, Harrison HB, Jones GP, Mansour H, Berumen ML (2015) Resolving genealogical relationships in the Pyjama cardinalfish, Sphaeramia nematoptera (Apogonidae) with 23 novel microsatellite markers. Conserv Genet Resour 7:623–626

    Article  Google Scholar 

  • Spalding MD, Ravilious C, Green EP (2001) World atlas of coral reefs. World Conservation Monitoring Centre, University of California Press, Berkeley, United Nations Environment Programme, 416

    Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690

    Article  CAS  PubMed  Google Scholar 

  • Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web-servers. Syst Biol 75:758–771

    Article  Google Scholar 

  • Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1:269–285

    CAS  PubMed  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Technelysium PL (2012) Chromas Lite version 2.1. South Brisbane, Queensland, Australia

  • Terry A, Bucciarelli G, Bernardi G (2000) Restricted gene flow and incipient speciation in disjunct Pacific Ocean and Sea of Cortez populations of a reef fish species, Girella nigricans. Evolution 54:652–659

    Article  CAS  PubMed  Google Scholar 

  • van Oosterhout C, Hutchinson WF, Derek PMW, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J Biogeogr 27:1153–1167

    Article  Google Scholar 

  • Ward RD, Zemlak TS, Innes BH, Last PR, Hebert PDN (2005) DNA barcoding Australia’s fish species. Phil Trans R Soc Lond B Biol Sci 360:1847–1857

    Article  CAS  Google Scholar 

  • Webster JA, Davies PJ (2003) Coral variation in tow deep drill cores: significance for the Pleistocene development of the Great Barrier Reef. Sediment Geol 159:61–80

    Article  Google Scholar 

  • Wellenreuther M, Clements KD (2008) Determinants of habitat association in a sympatric clade of marine fishes. Mar Biol 154:393–402

    Article  Google Scholar 

  • Zhu S, Degnan JH, Steel M (2011) Clades, clans, and reciprocal monophyly under neutral evolutionary models. Theor Popul Biol 79:220–227

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Mark O’Callaghan, Andreas Bally, Vanessa Miller-Sims, David Welsh, Naomi Gardiner and Felicity Smith for assistance with sample collection, and Susanne Wallenstein and students from the Marine Biological Laboratory, Woods Hole, USA, for helping to process samples. Photograph of O. doederleini (Fig. 5b) was taken by Andreas Bally. Thanks to Sebastian Schmidt Roach for helpful comments on the manuscript; Gabrielle Miller for improving the language style. This work was funded by National Science Foundation Grant OCE-0452885, the German Science Foundation (Ge 842/6-1) to G.G. and OCE-0452988 to J.A., National Geographic Society Grant 7236-02, and ARC Centre of Excellence for Coral Reef Studies grant (to M.J.K.).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gabriele Gerlach.

Additional information

Communicated by Ecology Editor Dr. Michael Berumen

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 757 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gerlach, G., Atema, J., Raupach, M.J. et al. Cryptic species of cardinalfish with evidence for old and new divergence. Coral Reefs 35, 437–450 (2016). https://doi.org/10.1007/s00338-015-1395-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00338-015-1395-7

Keywords

Navigation