Skip to main content

Advertisement

Log in

Eco-geographic units, population hierarchy, and a two-level conservation strategy with reference to a critically endangered salmonid, Sakhalin taimen Parahucho perryi

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

Abstract

Hierarchical population structure can result from range-wide geographic subdivision under conditions of environmental heterogeneity and weak gene flow. While a lower level of structure can be formed by local populations within eco-geographic regions, an upper level can be characterized by variation between populations from different regions, and thus, be represented by evolutionarily significant units (ESUs) defined by environmental, ecological and genetic variation. Selection of ESUs may depend on the sequence of using these three sources of variation. We propose to determine ESUs by first using non-genetic, ecological and geographical gradients for defining preliminary population groups (eco-geographic units, EGUs) and then testing whether the boundaries of these units are genetically coherent and thus represent ESUs or warrant their further modification. We evaluate this approach using Sakhalin taimen, an East Asian endangered endemic fish. Forty-one samples (473 fish) were drawn from thirty populations across the species range and genotyped at microsatellite DNA markers. We assign the populations into ESUs based on geographic and life history criteria and subsequent application of genetic diversity analyses. The ESUs appeared to be greatly diverged genetically. Within ESUs, local populations are genetically differentiated, have low effective sizes, show signatures of demographic decline and extremely restricted gene flow. Conservation plans aimed to restore or maintain a specific threatened population should take into account such hierarchical structure, and in particular be based on the genetic resources drawn from each population or using ecologically and genetically similar populations from the same ESU as donors for restoration of the population.

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

Similar content being viewed by others

References

  • Allendorf FW, Luikart GH, Aitken SN (2012) Conservation and the genetics of populations. Wiley & Sons, Chichester

  • Andrew RL, Bernatchez L, Bonin A, Buerkle CA, Carstens BC, Emerson BC, Garant D, Giraud T, Kane NC, Rogers SM (2013) A road map for molecular ecology. Mol Ecol 22:2605–2626

    Article  PubMed  Google Scholar 

  • Baillie J, Butcher ER, Commission ISS (2012) Priceless Or worthless?: The world’s most threatened species. Zoological Society of London, London

  • Dionne M, Caron F, Dodson JJ, Bernatchez L (2008) Landscape genetics and hierarchical genetic structure in Atlantic salmon: the interaction of gene flow and local adaptation. Mol Ecol 17:2382–2396

    Article  CAS  PubMed  Google Scholar 

  • Do C, Waples RS, Peel D, Macbeth G, 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 Res 14:209–214

    Article  CAS  Google Scholar 

  • Edo K, Kawaguchi Y, Nunokawa M, Kawamula H, Higashi S (2005) Morphology, stomach contents and growth of the endangered salmonid, Sakhalin taimen Hucho perryi, captured in the Sea of Okhotsk, northern Japan: evidence of an anadromous form. Environ Biol Fishes 74:1–7

    Article  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 

  • Falconer DS (1960) Introduction to quantitative genetics. Ronald Press Co., New York

    Google Scholar 

  • Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB (2011) Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity 106:404–420

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fukushima M, Shimazaki H, Rand PS, Kaeriyama M (2011) Reconstructing Sakhalin taimen Parahucho perryi historical distribution and identifying causes for local extinctions. Trans Am Fish Soc 140:1–13

    Google Scholar 

  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496

    Article  PubMed Central  PubMed  Google Scholar 

  • Gagnaire P-A, Normandeau E, Côté C, Hansen MM, Bernatchez L (2012) The genetic consequences of spatially varying selection in the panmictic American eel (Anguilla rostrata). Genetics 190:725–736

    Article  PubMed Central  PubMed  Google Scholar 

  • Gritsenko OF (2002) Diadromous Fishes of Sakhalin (Systematics, Ecology, Fisheries). VNIRO Publishing, Moscow, p 247 [in Russian]

    Google Scholar 

  • Honda K, Arai T, Takahashi N, Miyashita K (2010) Life history and migration of Sakhalin taimen, Hucho perryi, caught from Lake Akkeshi in eastern Hokkaido, Japan, as revealed by Sr: Ca ratios of otoliths. Ichthyol Res 57:416–421

    Article  Google Scholar 

  • Honda K, Kagiwada H, Takahashi N, Miyashita K (2012) Seasonal stream habitat of adult Sakhalin taimen, Parahucho perryi, in the Bekanbeushi River system, eastern Hokkaido, Japan. Ecol Fresw Fish 21:640–657

    Article  Google Scholar 

  • Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332

    Article  Google Scholar 

  • Lewis PO, Zaykin D (2001) Genetic data analysis: computer program for the analysis of allelic data (http//lewis.eeb.uconn.lewishome/software.html)

  • Manel S, Joost S, Epperson BK, Holderegger R, Storfer A, Rosenberg MS, Scribner KT, Bonin A, Fortin MJ (2010) Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field. Mol Ecol 19:3760–3772

    Article  CAS  PubMed  Google Scholar 

  • Martynenko AB (2007) Provisory regionalization of the Far East Federal district of the Russian Federation for zoogeographical purposes. In: Kurentsov AI (ed) Annual memorial meetings. The Far East National University, Vladivostok, 18, 29–47. [in Russian]

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

  • Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474

    Article  PubMed Central  PubMed  Google Scholar 

  • Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65

    Article  CAS  PubMed  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Pearse DE, Miller MR, Abadía-Cardoso A, Garza JC (2014) Rapid parallel evolution of standing variation in a single, complex, genomic region is associated with life history in steelhead/rainbow trout. Proc Royal Soc B 281(1783):20140012

    Article  Google Scholar 

  • Perrier C, Bourret V, Kent MP, Bernatchez L (2013) Parallel and nonparallel genome-wide divergence among replicate population pairs of freshwater and anadromous Atlantic salmon. Mol Ecol 22:5577–5593

    Article  CAS  PubMed  Google Scholar 

  • Piry S, Alapetite A, Cornuet J-M, Paetkau D, Baudouin L, Estoup A (2004) GENECLASS2: a software for genetic assignment and first-generation migrant detection. J Hereid 95:536–539

    Article  CAS  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pudovkin A, Zhdanova O, Hedgecock D (2010) Sampling properties of the heterozygote-excess estimator of the effective number of breeders. Cons Gen 11:759–771

    Article  Google Scholar 

  • Rand PS (2006) Hucho perryi. In: IUCN red list of threatened species. Version 2010.4. http://www.iucnredlist.org/apps/redlist/details/61333

  • Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci 94:9197–9201

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Safronov SN and Sukhonos PS (2006) Morphological features and the condition of populations of Sakhalin taimen (Parahucho perryi) in Dagi River (The Nyi Bay, Sakhalin Island). In: Economic, social, and ecological problems at the Okhotsk Sea and the ways of their solution. Petropavlovsk-Kamchatskiy State University, Petropavlovsk-Kamchatskiy, [in Russian]

  • Safronov SN, Nikitin VD, Sukhonos PS (2006) Current condition and conservation of populations of Sakhalin taimen Parahucho perryi in Sakhakin Island rivers. In: Economic enviromental sustainability for Sakhakin’s people and salmon. ANO “Sakhalin Salmon Initiative”, Yuzno-Sakhalinsk. [in Russian]

  • Semenchenko AYu, Zolotukhin SF (2011) Sakhalin taimen Parahucho perryi reproduction efficiency in Sakhalin rivers, and a strategy of its protection. Levanidov VYa Bienn Meml Meet 5:472–482 [in Russian]

    Google Scholar 

  • Smouse PE, Peakall R (1999) Spatial autocorrelation analysis of individual multiallele and multilocus genetic structure. Heredity 82:561–573

    Article  PubMed  Google Scholar 

  • Sork VL, Waits L (2010) Contributions of landscape genetics–approaches, insights, and future potential. Mol Ecol 19:3489–3495

    Article  PubMed  Google Scholar 

  • Waples RS (1991) Pacific salmon, Oncorhynchus spp., and the definition of “species” under the endangered species act. Mar Fish Rev 53:11–22

    Google Scholar 

  • Waples RS (2006) Distinct Population Segments. In: Scott JM, Goble DD, Davis FW (eds) The endangered species act at thirty: conserving biodiversity in human-dominated landscapes. Island Press, Washington DC, pp 127–149

    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 Central  PubMed  Google Scholar 

  • Waples RS, Gustafson RG, Weitkamp LA, Myers JM, Johnson OW, Busby PJ, Hard JJ, Baker B (2001) Characterizing diversity in Pacific salmon. J Fish Biol 59(Suppl A):1–41

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed Central  PubMed  Google Scholar 

  • Zaykin D, Zhivotovsky L, Weir B (1995) Exact tests for association between alleles at arbitrary numbers of loci. Genetica 96:169–178

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman CE, Rand PS, Fukushima M, Zolotukhin SF (2012) Migration of Sakhalin taimen (Parahucho perryi): evidence of freshwater resident life history types. Environ Biol Fishes 93:223–232

    Article  Google Scholar 

  • Zolotukhin SF, Semenchenko AYu (2008) Growth and distribution of Sakhalin taimen Parahucho perryi (Brevoort) in watersheds. Levanidov VYa Bienn Meml Meet 4:317–338 [in Russian]

    Google Scholar 

Download references

Acknowledgments

We are thankful to the Agency ‘Rosprirodnadzor’ for permissions to obtain genetic samples from Sakhalin taimen populations and to S. Didenko for setting up of field expeditions. We are indebted to D. Didenko (travel agency “Ostrov”) for his great help in sampling, as well as other samplers listed in Table A1. Field expeditions and genetic work were supported in part by Grants to L.Zh. from RAS program “Living Nature– Genofonds”, and from “Sakhalin Salmon Initiatives”; all participants were also supported by funds of their institutions, and P.R. by a Grant from National Geographic Society. We are grateful to Dr. Robin Waples and an anonymous reviewer for their valuable comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lev A. Zhivotovsky.

Additional information

Lev A. Zhivotovsky and Andrey A. Yurchenko have contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 162 kb)

Supplementary material 2 (DOCX 219 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhivotovsky, L.A., Yurchenko, A.A., Nikitin, V.D. et al. Eco-geographic units, population hierarchy, and a two-level conservation strategy with reference to a critically endangered salmonid, Sakhalin taimen Parahucho perryi . Conserv Genet 16, 431–441 (2015). https://doi.org/10.1007/s10592-014-0670-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-014-0670-4

Keywords

Navigation