Skip to main content


Log in

Going, going, gone: evidence for loss of an endemic species pair of threespine sticklebacks (Gasterosteus aculeatus) with implications for protection under species-at-risk legislation

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


Genomic extinction occurs when the unique combination of genetic traits that characterize distinct phenotypes are eliminated by introgressive hybridization even if population size is greater than zero. Benthic and limnetic threespine sticklebacks (Gasterosteus aculeatus) constitute reproductively isolated undescribed biological species that have evolved independently in several lakes in southwestern British Columbia, Canada (known as “species pairs” in each lake). Here we investigated whether the two species that comprise the pair from Enos Lake, southeastern Vancouver Island, remain as two distinct gene pools. Multi-season samples (>1200 fish) obtained over two years from throughout the lake and assayed for variation in morphological traits characteristic of the two species (i.e., body depth, dorsal spine count, gill raker counts) and at 12 microsatellite DNA loci consistently indicated the existence of only a single group of sticklebacks. There was no consistent evidence of two groups in any morphological trait, and mean gill raker counts were consistently intermediate (20–21) to those of known benthics (~18) and limnetics (~24) which together comprised strikingly bimodal distributions in historical samples. Genetic analyses employing model-based clustering also consistently indicated the presence of only a single genetic group of sticklebacks. Compared to historical samples and to benthics and limnetics from other lakes, no Enos Lake fish could be identified confidently as a pure benthic or limnetic. Our results provide the strongest evidence yet that the Enos Lake sticklebacks now consist of a single morphological and genetic population of sticklebacks, that the unique combination of genetic and morphological traits that characterized benthic and limnetic sticklebacks no longer exist, and that their current status under Canada’s Species-at Risk Act as Endangered should be re-evaluated.

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

Similar content being viewed by others


  • Allendorf FW, Leary RF, Hitt NP, Knudsen KL, Lundquist LL, Spruell P (2004) Intercrosses and the US Endangered Species Act: should hybridized populations be included as westslope cutthroat trout? Conserv Biol 18:1203–1213

    Article  Google Scholar 

  • Austin MA, Buffett DA, Nicolson DJ, Scudder GGE, Stevens V (eds) (2008) Taking nature’s pulse: the status of biodiversity in British Columbia. Biodiversity BC, Victoria. Accessed 12 Oct 2014

  • Barrett RD, Paccard A, Healy TM, Bergek S, Schulte PM, Schluter D, Rogers SM (2011) Rapid evolution of cold tolerance in stickleback. Proc Roy Soc Lond B 278:233–238

    Article  Google Scholar 

  • Behm JE, Ives AR, Boughman JW (2010) Breakdown in postmating isolation and the collapse of a species pair through hybridization. Am Nat 17:11–26

    Article  Google Scholar 

  • Bell MA, Aguirre WE, Buck NJ (2004) Twelve years of contemporary armor evolution in a threespine stickleback population. Evolution 58:814–824

    Article  PubMed  Google Scholar 

  • Bentzen P, McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): specialization for alternative trophic niches in the Enos Lake species pair. Can J Zool 62:2280–2286

    Article  Google Scholar 

  • Bentzen P, Ridgway MS, McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): spatial segregation and seasonal habitat shifts in the Enos Lake species pair. Can J Zool 62:2436–2439

    Article  Google Scholar 

  • Cooper IA, Gilman RT, Boughman JW (2011) Sexual dimorphism and speciation on two ecological coins: patterns from nature and theoretical predictions. Evolution Int J org Evolution 65:2553–2571

    Article  Google Scholar 

  • COSEWIC (2013) COSEWIC assessment and update status report on the Enos Lake benthic and limnetic threespine sticklebacks (Gasterosteus aculeatus) in Canada. Committee on the Status of Endangered Wildlife in Canada.

  • COSEWIC (2016) Committee on the status of endangered wildlife in Canada. Operations and procedures manual. Environment and Climate Change Canada, Canadian Wildlife Service, Ottawa

  • Culotta E, Pennisi E (2005) Evolution in action. Science 310:1878–1879

    Article  CAS  PubMed  Google Scholar 

  • Day T, Pritchard J, Schluter D (1994) A comparison of two sticklebacks. Evolution 48:1723–1734

    Article  PubMed  Google Scholar 

  • Dextrase A, Mandrak N (2006) Impacts of alien invasive species on freshwater fauna at risk in Canada. Biol Invasions 8:13–24

    Article  Google Scholar 

  • Dudgeon D, Arthington AH, Gessner MO, Kawabata Z-I, Knowler DJ, Lévêque CL, Naiman RJ, Prieur-Richard AH, Soto D, Stiassny MLJ, Sullivan CA (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81:163–182

    Article  PubMed  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gilman RT, Behm JE (2011) Hybridization, species collapse, and species reemergence after disturbance to premating mechanisms of reproductive isolation. Evolution 65:2592–2605

    Article  PubMed  Google Scholar 

  • Gow JL, Peichel CL, Taylor EB (2006) Contrasting hybridization rates between sympatric three-spined sticklebacks highlight the fragility of reproductive barriers between evolutionarily young species. Mol Ecol 15:739–752

    Article  PubMed  Google Scholar 

  • Gow JL, Rogers SM, Jackson M, Schluter D (2008) Ecological predictions lead to the discovery of a benthic-limnetic species pair of threespine stickleback in Little Quarry Lake, British Columbia. Can J Zool 86:564–571

    Article  Google Scholar 

  • Gynther I, Waller N, Leung LK-P (2016) Confirmation of the extinction of the Bramble Cay melomys Melomys rubicola on Bramble Cay, Torres Strait: results and conclusions from a comprehensive survey in August–September 2014. Unpublished report to the Department of Environment and Heritage Protection, Queensland Government, Brisbane.

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

    Google Scholar 

  • IUCN Standards and Petitions Subcommittee (2010) Guidelines for Using the IUCN Red List Categories and Criteria. Version. Prepared by the Standards and Petitions Subcommittee in March 2010. Accessed 17 Jan 2017

  • Jones FC, Chan YF, Schmutz J, Grimwood J, Brady SD, Southwick AM, Absher DM, Myers RM, Reimchen TE, Deagle BE, Schluter D (2012) A genome-wide SNP genotyping array reveals patterns of global and repeated species-pair divergence in sticklebacks. Curr Biol 22:83–90

    Article  CAS  PubMed  Google Scholar 

  • Kitano J, Bolnick DI, Beauchamp DA, Mazur MM, Mori S, Nakano T, Peichel CL (2008) Reverse evolution of armor plates in the threespine stickleback. Curr Biol 18:769–774

    Article  CAS  PubMed  Google Scholar 

  • Klepaker T (1993) Morphological changes in a marine population of threespined stickleback, Gasterosteus aculeatus, recently isolated in fresh water. Can J Zool 71:1251–1258

    Article  Google Scholar 

  • Kraak SBM, Mundwiler B, Hart PJB (2001) Increased number of hybrids between benthic and limnetic three-spined sticklebacks in Enos Lake, Canada; the collapse of a species pair? J Fish Biol 58:1458–1464

    Article  Google Scholar 

  • Lavin PA, McPhail JD (1985) The evolution of freshwater diversity in the threespine stickleback (Gasterosteus aculeatus): site-specific differentiation of trophic morphology. Can J Zool 63:2632–2638

    Article  Google Scholar 

  • Leaver SD, Reimchen TE (2012) Abrupt changes in defence and trophic morphology of the giant threespine stickleback (Gasterosteus sp.) following colonization of a vacant habitat. Biol J Linn Soc 107:494–509

    Article  Google Scholar 

  • Malek TB, Boughman JW, Dworkin I, Peichel K (2012) Admixture mapping of male nuptial colour and body shape in a recently formed hybrid population of threespine stickleback. Mol Ecol 21:5265–5279

    Article  PubMed Central  PubMed  Google Scholar 

  • McGee MD, Schluter D, Wainwright PC (2013) Functional basis of ecological divergence in sympatric stickleback. BMC Evol Biol 13:277

    Article  PubMed Central  PubMed  Google Scholar 

  • McKinnon JS, Rundle HD (2002) Speciation in nature: the threespine stickleback model systems. Trends Ecol Evol 17:480–488

    Article  Google Scholar 

  • McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Enos Lake, Vancouver Island, British Columbia. Can J Zool 62:1402–1408

    Article  Google Scholar 

  • McPhail JD (1992) Ecology and evolution of sympatric sticklebacks (Gasterosteus): evidence for a species-pair in Paxton Lake, Texada Island, British Columbia. Can J Zool 70:361–369

    Article  Google Scholar 

  • McPhail JD (1993) Ecology and evolution of sympatric sticklebacks (Gasterosteus): origin of the species pairs. Can J Zool 71:515–523

    Article  Google Scholar 

  • McPhail JD (1994) Speciation and the evolution of reproductive isolation in the sticklebacks (Gasterosteus) of south-western British Columbia. In: Bell MA, Foster SA (eds) Evolutionary biology of the threespine stickleback. Oxford University Press, Oxford, pp 399–437

    Google Scholar 

  • McPhail JD (2007) The freshwater fishes of British Columbia. University of Alberta Press, Edmonton

    Google Scholar 

  • Nosil P, Reimchen TE (2005) Ecological opportunity and levels of morphological variance within freshwater stickleback populations. Biol J Linn Soc 86:297–308

    Article  Google Scholar 

  • Ridgway MS, McPhail JD (1984) Ecology and evolution of sympatric sticklebacks (Gasterosteus): mate choice and reproductive isolation in the Enos Lake species pair. Can J Zool 62:1813–1818

    Article  Google Scholar 

  • Rundle HD, Nagel L, Boughman JW, Schluter D (2000) Natural selection and parallel speciation in sympatric sticklebacks. Science 287:306–308

    Article  CAS  PubMed  Google Scholar 

  • SARA (2003) Species at risk act (S.C. 2002, c. 29). Canadian Department of Justice, Ottawa. Available at

  • Schluter D, McPhail JD (1992) Ecological character displacement and speciation in sticklebacks. Am Nat 140:85–108

    Article  CAS  PubMed  Google Scholar 

  • Taylor EB, McPhail JD (2000) Historical contingency and ecological determinism interact to prime speciation in sticklebacks, Gasterosteus. Proc Roy Soc Lond B 267:2375–2384

    Article  CAS  Google Scholar 

  • Taylor EB, Boughman JW, Groenenboom M, Sniatynski M, Schluter D, Gow JL (2006) Speciation in reverse: morphological and genetic evidence of the collapse of a three-spined stickleback (Gasterosteus aculeatus) species pair. Mol Ecol 15:343–355

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Velema GJ, Rosenfeld JR, Taylor EB (2012) Effects of invasive American signal crayfish (Pacifastacus leniusculus) on the reproductive behaviour of threespine stickleback (Gasterosteus aculeatus) sympatric species pairs). Can J Zool 90:1328–1338

    Article  Google Scholar 

Download references


The cooperation of the BC Ministry of Environment, Fisheries and Oceans Canada (Pacific Region), and Dave Scott of Fairwinds Real Estate Management, Inc. is greatly appreciated. We thank Elias Elhaimer for assistance with morphological measurements and Sara Miller and Dolph Schluter for provision of samples from Murdo Fraser Pond. The manuscript benefitted from helpful commentary by two anonymous reviewers and C. Garza.


Funding for this project was provided by the Natural Sciences and Engineering Research Council of Canada (Discovery and Equipment Grant Programs) and the BC Ministry of Environment in the form of grants awarded to EBT.

Author information

Authors and Affiliations


Corresponding author

Correspondence to Eric B. Taylor.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 10 KB)

Supplementary material 2 (PDF 638 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Taylor, E.B., Piercey, R.S. Going, going, gone: evidence for loss of an endemic species pair of threespine sticklebacks (Gasterosteus aculeatus) with implications for protection under species-at-risk legislation. Conserv Genet 19, 297–308 (2018).

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: