Skip to main content

Advertisement

SpringerLink
Log in

Effective population size and heterozygosity-fitness correlations in a population of the Mediterranean lagoon ecotype of long-snouted seahorse Hippocampus guttulatus

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

The management of endangered species is complicated in the marine environment owing to difficulties to directly access, track and monitor in situ. Population genetics provide a genuine alternative to estimate population size and inbreeding using non-lethal procedures. The long-snouted seahorse, Hippocampus guttulatus, is facing multiple threats such as human disturbance or by-catch, and has been listed in the red list of IUCN. One large population is found in the Thau lagoon, in the south of France. A recent study has shown this population belongs to a genetic lineage only found in Mediterranean lagoons that can be considered as an Evolutionarily Significant Unit (ESU) and should be managed with dedicated conservation strategies. In the present study, we used genetic analysis of temporal samples to estimate the effective population size of the Thau population and correlations between individual multilocus heterozygosity and fitness traits to investigate the possible expression of inbreeding depression in the wild. Non-invasive sampling of 172 seahorses for which profiles were pictured and biometric data recorded were genotyped using 291 informative SNPs. Genetic diversity remained stable over a 7-year time interval. In addition, very low levels of close relatedness and inbreeding were observed, with only a single pair of related individuals in 2008 and two inbreds in 2013. We did not detect departure from identity equilibrium. The effective population size was estimated to be Ne = 2742 (~ 40 reproductive seahorses per km2), larger than previously thought. No correlation was observed between heterozygosity and fluctuating asymmetry or other morphometric traits, suggesting a population with low variance in inbreeding. Together these results suggest this population does not meet conventional genetic criteria of an endangered population, as the population seems sufficiently large to avoid inbreeding and its detrimental effects. This study paves the way for the genetic monitoring of this recently discovered ESU of a species with patrimonial and conservation concerns.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Balloux F, Amos W, Coulson T (2004) Does heterozygosity estimate inbreeding in real populations? Mol Ecol 13:3021–3031

    Article  CAS  PubMed  Google Scholar 

  • Bierne N, Tsitrone A, David P (2000) An inbreeding model of associative overdominance during a population bottleneck. Genetics 155:1981–1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broquet T, Viard F, Yearsley JM (2013) Genetic drift and collective dispersal can result in chaotic genetic patchiness. Evolution 67:1660–1675

    Article  PubMed  Google Scholar 

  • Caldwell IR, Vincent ACJ (2012) A sedentary fish on the move: effects of displacement on long-snouted seahorse (Hippocampus guttulatus Cuvier) movement and habitat use. Environ Biol Fishes 96:67–75

    Article  Google Scholar 

  • Caughley G (1994) Directions in conservation biology. J Anim Ecol 63:215–244

    Article  Google Scholar 

  • Chapman RW, Ball AO, Mash LR (2002) Spatial homogeneity and temporal heterogeneity of red drum (Sciaenops ocellatus) microsatellites: effective population sizes and management implications. Mar Biotechnol 4:589–603

    Article  CAS  Google Scholar 

  • Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC (2009) A quantitative review of heterozygosity-fitness correlations in animal populations. Mol Ecol 18:2746–2765

    Article  CAS  PubMed  Google Scholar 

  • Claude J (2008) Morphometrics with R. Springer, New York

    Google Scholar 

  • Correia M, Caldwell IR, Koldewey HJ, Andrade JP, Palma J (2015) Seahorse (Hippocampinae) population fluctuations in the Ria Formosa Lagoon, south Portugal. J Fish Biol 87:679–690

    Article  CAS  PubMed  Google Scholar 

  • Curtis JMR (2007) Validation of a method for estimating realized annual fecundity in a multiple spawner, the long-snouted seahorse (Hippocampus guttulatus), using underwater visual census. Fish Bull 105:327–337

    Google Scholar 

  • Curtis JMR, Vincent ACJ (2006) Life history of an unusual marine fish: survival, growth and movement patterns of Hippocampus guttulatus Cuvier 1829. J Fish Biol 68:707–733

    Article  Google Scholar 

  • David P (1998) Heterozygosity–fitness correlations: new perspectives on old problems. Heredity 80:531–537

    Article  PubMed  Google Scholar 

  • David P, Pujol B, Viard F, Castella V, Goudet J (2007) Reliable selfing rate estimates from imperfect population genetic data. Mol Ecol 16:2474–2487

    Article  CAS  PubMed  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth GM, Tillett BJ, Ovenden JR (2014) NeEstimator v2: re-implementation of software for the estimation of contemporary effective population size (Ne) from genetic data. Mol Ecol Resour 14:209–214

    Article  CAS  PubMed  Google Scholar 

  • Doyle J, Doyle J (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15

    Google Scholar 

  • Dryden IL, Mardia KV (1998) Statistical shape analysis. Wiley, Chichester, p XIX-5

    Google Scholar 

  • Foster SJ, Vincent ACJ (2004) Life history and ecology of seahorses: implications for conservation and management. J Fish Biol 65:1–61

    Article  Google Scholar 

  • Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327

    Article  CAS  PubMed  Google Scholar 

  • Fraser DJ, Hansen MM, Østergaard S, Tessier N, Legault M, Bernatchez L (2007) Comparative estimation of effective population sizes and temporal gene flow in two contrasting population systems. Mol Ecol 16:3866–3889

    Article  PubMed  Google Scholar 

  • Gamito S (2008) Three main stressors acting on the Ria Formosa lagoonal system (Southern Portugal): physical stress, organic matter pollution and the land–ocean gradient. Estuar Coast Shelf Sci 77:710–720

    Article  Google Scholar 

  • Garrick-Maidment N, Trewhella S, Hatcher J, Collins KJ, Mallinson JJ (2010) Seahorse tagging project, Studland Bay, Dorset UK. Mar Biodivers Rec 3:e73

    Article  Google Scholar 

  • Gilbert KJ, Whitlock MC (2015) Evaluating methods for estimating local effective population size with and without migration. Evolution 69:2154–2166

    Article  PubMed  Google Scholar 

  • Hare MP, Nunney L, Schwartz MK, Ruzzante DE, Burford M, Waples RS, Ruegg K, Palstra F (2011) Understanding and estimating effective population size for practical application in marine species management. Conserv Biol 25:438–449

    Article  PubMed  Google Scholar 

  • Hendriks IE, Duarte CM, Heip CHR (2006) Biodiversity research still grounded. Science 312:1715

    Article  CAS  PubMed  Google Scholar 

  • Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium1. Genet Resour 38:209–216

    Article  Google Scholar 

  • Hoarau G, Boon E, Jongma DN, Ferber S, Palsson J, der Veer HWV, Rijnsdorp AD, Stam WT, Olsen JL (2005) Low effective population size and evidence for inbreeding in an overexploited flatfish, plaice (Pleuronectes platessa L.). Proc R Soc Lond B 272:497–503

    Google Scholar 

  • Keenan K, McGinnity P, Cross TF, Crozier WW, Prodöhl PA (2013) diveRsity: an R package for the estimation and exploration of population genetics parameters and their associated errors. Methods Ecol Evol 4:782–788

    Article  Google Scholar 

  • López A, Vera M, Planas M, Bouza C (2015) Conservation genetics of threatened Hippocampus guttulatus in vulnerable habitats in NW Spain: temporal and spatial stability of wild populations with flexible polygamous mating system in captivity. PLoS ONE 10:e0117538

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lotze HK, Lenihan HS, Bourque BJ, Bradbury RH, Cooke RG, Kay MC, Kidwell SM, Kirby MX, Peterson CH, Jackson JBC (2006) Depletion, degradation, and recovery potential of estuaries and coastal seas. Science 312:1806–1809

    Article  CAS  PubMed  Google Scholar 

  • Louisy P, Bérenger L (2015) Hippocampes et syngnathes du Golfe du Lion: état des connaissances. Association Peau-Bleue - Agence des aires marines protégées, 94p

  • Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    Article  CAS  Google Scholar 

  • Palmer AR (1994) Fluctuating asymmetry analyses: a primer. In: Markow TA (ed) Developmental instability: its origins and evolutionary implications: proceedings of the international conference on developmental instability: its origins and evolutionary implications, Tempe, Arizona, 14–15 June 1993. Springer, Dordrecht, pp 335–364

    Chapter  Google Scholar 

  • Pérez-Ruzafa A, Marcos C, Pérez-Ruzafa IM (2011) Developmental instability: its origins and evolutionary implications: proceedings of the international conference on developmental instability: its origins and evolutionary implications, Tempe, Arizona, 14–15 June 1993. Phys Chem Earth Parts ABC 36:160–166

    Article  Google Scholar 

  • R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Riquet F, Le Cam S, Fonteneau E, Viard F (2016) Moderate genetic drift is driven by extreme recruitment events in the invasive mollusk Crepidula fornicata. Heredity 117:42–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riquet F, Liautard-Haag C, Woodall L, Bouza C, Louisy P, Hamer B, Otero-Ferrer F, Aublanc P, Béduneau V, Briard O, El Ayari T, Hochscheid S, Belkhir K, Arnaud-Haond S, Gagnaire P-A, Bierne N (2019) Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages. Evolution 73:817–835

    Article  PubMed  Google Scholar 

  • Rohlf FJ (2010) tpsDig. Stony Brook, Department of Ecology and Evolution, State University of New York, NY

    Google Scholar 

  • Rohlf FJ, Slice D (1990) Extensions of the procrustes method for the optimal superimposition of landmarks. Syst Biol 39:40–59

    Google Scholar 

  • Romiguier J et al (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature 515:261–263

    Article  CAS  PubMed  Google Scholar 

  • Rousset F (2008) genepop’007: a complete re-implementation of the genepop software for Windows and Linux. Mol Ecol Resour 8:103–106

    Article  PubMed  Google Scholar 

  • Roux C, Fraïsse C, Romiguier J, Anciaux Y, Galtier N, Bierne N (2016) Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biol 14:e2000234

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Slate J, David P, Dodds KG, Veenvliet BA, Glass BC, Broad TE, McEwan JC (2004) Understanding the relationship between the inbreeding coefficient and multilocus heterozygosity: theoretical expectations and empirical data. Heredity 93:255–265

    Article  CAS  PubMed  Google Scholar 

  • Spearman C (1904) “General intelligence”, objectively determined and measured. Am J Psychol 15:201–292

    Article  Google Scholar 

  • Szulkin M, Bierne N, David P (2010) Heterozygosity-fitness correlations: a time for reappraisal. Evolution 64:1202–1217

    PubMed  Google Scholar 

  • Teles-Machado A, Peliz Á, Dubert J, Sánchez RF (2007) On the onset of the Gulf of Cadiz Coastal countercurrent. Geophys Res Lett 34:L12601

    Article  Google Scholar 

  • Traill LW, Brook BW, Frankham RR, Bradshaw CJA (2010) Pragmatic population viability targets in a rapidly changing world. Biol Conserv 143:28–34

    Article  Google Scholar 

  • Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genet Resour 78:243–257

    Article  CAS  Google Scholar 

  • Wang J (2007) Triadic IBD coefficients and applications to estimating pairwise relatedness. Genet Res 89:135–153

    Article  CAS  PubMed  Google Scholar 

  • Wang J (2011) COANCESTRY: A program for simulating, estimating and analysing relatedness and inbreeding coefficients. Molecular EcologyResources 11:141–145

    Google Scholar 

  • Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waples RS (1998) Separating the wheat from the chaff: patterns of genetic differentiation in high gene flow species. J Hered 89:438–450

    Article  Google Scholar 

  • Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352

    Article  CAS  PubMed  Google Scholar 

  • Waples RS (2006) Seed banks, salmon, and sleeping genes: effective population size in semelparous, age-structured species with fluctuating abundance. Am Nat 167:118–135

    Article  PubMed  Google Scholar 

  • Waples RS, Do C (2008) ldne: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756

    Article  PubMed  Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    Article  PubMed  Google Scholar 

  • Wilks SS (1932) Certain generalizations in the analysis of variance. Biometrika 24:471–494

    Article  Google Scholar 

  • Woodall LC, Jones R, Zimmerman B, Guillaume S, Stubbington T, Shaw P, Koldewey HJ (2012) Partial fin-clipping as an effective tool for tissue sampling seahorses, Hippocampus spp. J Mar Biol Assoc U K 92:1427–1432

    Article  Google Scholar 

  • Woodall LC, Koldewey HJ, Boehm JT, Shaw PW (2015) Past and present drivers of population structure in a small coastal fish, the European long snouted seahorse Hippocampus guttulatus. Conserv Genet 16:1–15

    Article  Google Scholar 

  • Yearsley JM, Viard F, Broquet T (2013) The effect of collective dispersal on the genetic structure of a subdivided population. Evolution 67:1649–1659

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We are very grateful to local citizens, especially fishermen and divers, for their great help in collecting the fin samples used in this work. This work was funded by Languedoc-Roussillon Region “Chercheur(se)s d’avenir” (Connect7 project), by a LabEx CeMEB postdoctoral fellowship to FR, by Chocolaterie Guylian and a Natural Environment Research Council Industrial Case studentship (NER/S/C/2005/13461) to LW, and by a Fondation Nature & Découvertes grant to association Peau-Bleue and PL.

Author information

Authors and Affiliations

  1. ISEM, Univ Montpellier, CNRS, EPHE, IRD, Montpellier, France

    Florentine Riquet, Cathy Lieutard-Haag, Giulia Serluca, Julien Claude & Nicolas Bierne

  2. Department of Zoology, University of Oxford, John Krebs Field Station, Wytham, OX2 8QJ, UK

    Lucy Woodall

  3. Natural History Museum, Cromwell Road, London, SW7 5BD, UK

    Lucy Woodall

  4. ECOMERS Laboratory, Faculty of Sciences, University of Nice Sophia Antipolis, Parc Valrose, Nice, France

    Patrick Louisy

  5. Association Peau-Bleue, 46 Rue des Escais, Agde, France

    Patrick Louisy

Authors
  1. Florentine Riquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cathy Lieutard-Haag
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giulia Serluca
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lucy Woodall
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Julien Claude
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Patrick Louisy
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Nicolas Bierne
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Florentine Riquet.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Riquet, F., Lieutard-Haag, C., Serluca, G. et al. Effective population size and heterozygosity-fitness correlations in a population of the Mediterranean lagoon ecotype of long-snouted seahorse Hippocampus guttulatus. Conserv Genet 20, 1281–1288 (2019). https://doi.org/10.1007/s10592-019-01210-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-019-01210-3

Keywords

Search

Navigation