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Conservation Genetics

, Volume 19, Issue 2, pp 265–274 | Cite as

Fine-scale differences in genetic and census population size ratios between two stream fishes

  • T. A. Bernos
  • M. C. Yates
  • D. J. Fraser
Research Article

Abstract

Comparing the ratio of effective number of breeders (N b ) to adult population size (N) among closely related coexisting species can provide insights into the role of life history on N b /N ratios and inform conservation programs towards limiting the loss of evolutionary potential in natural populations. We estimated N b and N in two coexisting salmonid fishes (Brook trout and Atlantic salmon) for 3–4 consecutive years in two small, adjacent streams in Newfoundland, Canada, using mark-recapture (N), linkage disequilibrium (N b(LD)), and sibship frequency approaches (N b(Sib) ). We found that N b /N ratios were about 20-fold greater in Atlantic salmon than in brook trout (mean 0.20, range 0.06–0.56 vs. mean 0.02, range 0.01–0.05, respectively). This difference was consistent across N b estimators. In addition, we found that removing migrants reduced N b : the strength of the effect was weak for N b(LD) and much stronger for N b(Sib). Our results highlight the importance of subtle ecological differences and gene flow in shaping N b /N. They also provide some evidence that the linkage between demographic and evolutionary processes varies between closely related taxa and suggest that a more complete understanding of the N b /N range across various species is an important component of conservation genetics and management.

Keywords

Census population size Effective number of breeders Genetic monitoring Mark-recapture Salmonid 

Notes

Acknowledgements

We thank S. Smart, P. Debes, J-M. Matte, K. Marin and M. Heath for fieldwork, as well as Dr. John Carlos Garza and two anonymous reviewers for their helpful comments on previous versions of this manuscript. This research was funded by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant and Accelerator Award to D.J. Fraser, a Vladimir J. Elgart Graduate Entrance Scholarship and two Quebec Center for Biodiversity Science (QCBS) awards to T.A. Bernos, and an NSERC PGS Scholarship to M. Yates.

Supplementary material

10592_2017_997_MOESM1_ESM.docx (40 kb)
Supplementary material 1 (DOCX 39 KB)

References

  1. Anderson EC, Dunham KK (2008) The influence of family groups on inferences made with the program Structure. Mol Ecol Resour 8:1219–1229CrossRefPubMedGoogle Scholar
  2. Ardren WR, Kapuscinski AR (2003) Demographic and genetic estimates of effective population size (Ne) reveals genetic compensation in steelhead trout. Mol Ecol 12:35–49CrossRefPubMedGoogle Scholar
  3. Belmar-Lucero S, Wood J, Scott S et al (2012) Concurrent habitat and life history influences on effective/census population size ratios in stream-dwelling trout. Ecol Evol 2:563–573CrossRefGoogle Scholar
  4. Bernos TA, Fraser DJ (2016) Spatiotemporal relationship between adult census size and genetic population size across a wide population size gradient. Mol Ecol 25:4472–4487CrossRefPubMedGoogle Scholar
  5. Blanchfield PJ, Ridgway MS (1997) Reproductive timing and use of redd sites by lake-spawning brook trout (Salvelinus fontinalis). Can J Fish Aquatic Sci 54:747–756CrossRefGoogle Scholar
  6. Blanchfield PJ, Ridgway MS (2005) The relative influence of breeding competition and habitat quality on female reproductive success in lacustrine brook trout (Salvelinus fontinalis). Can J Fish Aquatic Sci 62:2694–2705CrossRefGoogle Scholar
  7. Consuegra S, Verspoor E, Knox D, García De Leániz C (2005) Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations. Conserv Genet 6:823–842CrossRefGoogle Scholar
  8. Curry RA, Neakes DLG (1995) Groundwater and the selection of spawning sites by brook trout (Salvelinus fontinalis). Can J Aquatic Sci 52:1733–1740CrossRefGoogle Scholar
  9. Curry RA, Noakes DLG, Curry RA, Neakes DLG (1995) Groundwater and the selection of spawning sites by brook trout (Salvelinus fontinalis). Can J Fish Aquatic Sci 52:1733–1740CrossRefGoogle Scholar
  10. Earl DA, VonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  11. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620CrossRefPubMedGoogle Scholar
  12. Ferchaud A-L, Perrier C, April J et al (2016) Making sense of the relationships between Ne, Nb and Nc towards defining conservation thresholds in Atlantic salmon (Salmo salar). Heredity 117:268–278CrossRefPubMedPubMedCentralGoogle Scholar
  13. Fleming IA (1996) Reproductive strategies of Atlantic salmon: ecology and evolution. Rev Fish Biol Fisheries 6:379–416CrossRefGoogle Scholar
  14. Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107CrossRefGoogle Scholar
  15. Frankham R, Bradshaw CJ, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, red list criteria and population viability analyses. Biol Conserv 170:56–63CrossRefGoogle Scholar
  16. Fraser DJ, Lippe C, Bernatchez L (2004) Consequences of unequal population size, asymmetric gene flow and sex-biased dispersal on population structure in brook charr (Salvelinus fontinalis). Mol Ecol 13:67–80CrossRefPubMedGoogle Scholar
  17. Gibson RJ, Williams DD, McGowan C, Davidson WS (1996) The ecology of dwarf fluvial Atlantic salmon, Salmo Salar L., cohabiting with brook trout, Salvelinus fontinalis (Mitchill), in Southeastern Newfoundland, Canada. Polskie Arch Hidrobiol 43:145–166Google Scholar
  18. Gilbert KJ, Whitlock MC (2015) Evaluating methods for estimating local effective population size with and without migration. Evol Int J Org Evol 69:2154–2166CrossRefGoogle Scholar
  19. Gomez-Uchida D, Knight TW, Ruzzante DE (2009) Interaction of landscape and life history attributes on genetic diversity, neutral divergence and gene flow in a pristine community of salmonids. Mol Ecol 18:4854–4869CrossRefPubMedGoogle Scholar
  20. Gomez-Uchida D, Palstra FP, Knight TW, Ruzzante DE (2013) Contemporary effective population and metapopulation size (Ne and meta-Ne): comparison among three salmonids inhabiting a fragmented system and differing in gene flow and its asymmetries. Ecol Evol 3:569–580CrossRefPubMedPubMedCentralGoogle Scholar
  21. Guillemette F, Vallee C, Bertolo A, Magnan P (2011) The evolution of redd site selection in brook charr in different environments†¯: same cue, same benefit for fitness. Freshw Biol 56:1017–1029CrossRefGoogle Scholar
  22. Hearn WE (1987) Interspecific competition and habitat segregation among stream-dwelling trout and salmon: a review. Fisheries 12:24–31CrossRefGoogle Scholar
  23. Hua YG, Orban L (2005) A simple and affordable method for high throughput DNA extraction from animal tissues for PCR. Electrophoresis 26:3081–3083CrossRefGoogle Scholar
  24. Hutchings JA (1993) Adaptive life histories effected by age-specific survival and growth rate. Ecology 74:673–684CrossRefGoogle Scholar
  25. Hutchings JA (1994) Age- and size- specific costs of reproduction within populations of brook trout, Salvelinus fontinalis. Nordic Soc Oikos 70:12–20CrossRefGoogle Scholar
  26. Jones OR, Wang J (2010) COLONY: A program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555CrossRefPubMedGoogle Scholar
  27. Kanno Y, Letcher BH, Hitt NP et al (2015) Seasonal weather patterns drive population vital rates and persistence in a stream fish. Global Change Biol 21:1856–1870CrossRefGoogle Scholar
  28. Kanno Y, Pregler KC, Hitt NP et al (2016) Seasonal temperature and precipitation regulate brook trout young-of-the-year abundance and population dynamics. Freshw Biol 61:88–99CrossRefGoogle Scholar
  29. King TL, Eackles MS, Letcher BH (2005) Microsatellite DNA markers for the study of Atlantic salmon (Salmo salar) kinship, population structure, and mixed-fishery analyses. Mol Ecol Notes 5:130–132CrossRefGoogle Scholar
  30. 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 11:355–373CrossRefGoogle Scholar
  31. Macmillan JL, Caissie D, Marshall TJ, Hinks L (2008) Population indices of brook trout (Salvelinus fontinalis), Atlantic salmon (Salmo salar), and salmonid competitors in relation to summer water temperature and habitat parameters in 100 streams in Nova Scotia. Can Tech Rep Fish Aquat Sci 2819:41Google Scholar
  32. Myhre AM, Engen S, Sæther B (2016) Effective size of density-dependent populations in fluctuating environments. Evol Int J Org Evol 70:2431–2446CrossRefGoogle Scholar
  33. Osborne MJ, Davenport SR, Hoagstrom CW, Turner TF (2010) Genetic effective size, Ne, tracks density in a small freshwater cyprinid, Pecos bluntnose shiner (Notropis simus pecosensis). Mol Ecol 19:2832–2844CrossRefPubMedGoogle Scholar
  34. Palstra FP, Fraser DJ (2012) Effective/census population size ratio estimation: a compendium and appraisal. Ecol Evol 2:2357–2365CrossRefPubMedPubMedCentralGoogle Scholar
  35. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: What can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447CrossRefPubMedGoogle Scholar
  36. Paterson S, Piertney SB, Knox D, Gilbey J, Verspoor E (2004) Characterization and PCR multiplexing of novel highly variable tetranucleotide Atlantic salmon (Salmo solar L.) microsatellites. Mol Ecol Notes 4:160–162CrossRefGoogle Scholar
  37. Perrier C, Normandeau E, Dionne M, Richard A, Bernatchez L (2014) Alternative reproductive tactics increase effective population size and decrease inbreeding in wild Atlantic salmon. Evol Appl 7:1094–1106CrossRefPubMedPubMedCentralGoogle Scholar
  38. Petersen C (1985) The yearly immigration of young plaice into the Limfjord from the German Sea. Rep Dan Biol Stn 5:5–84Google Scholar
  39. Phillipsen I, Funk W, Hoffman E, Monsen KJ, Blouin MS (2011) Comparative analyses of effective population size within and among species: ranid frogs as a case study. Evol Int J org Evol 65:2927–2946CrossRefGoogle Scholar
  40. Piry S, Alapetite A, Cornuet JM et al (2004) GENECLASS2: a software for genetic assignment and first-generation migrat detection. J Hered 95:536–539CrossRefPubMedGoogle Scholar
  41. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genet Soc Am 155:945–959Google Scholar
  42. Rannala B, Mountain JL (1997) Detecting immigration by using multilocus genotypes. Proc Natl Acad Sci 94:9197–9201CrossRefPubMedPubMedCentralGoogle Scholar
  43. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249CrossRefGoogle Scholar
  44. Ryan P, Kerekes J (1988) Characteristics of sport fish populations in six experimentally fished Salmonid lakes of Gros Morne National Park, Newfoundland. Canadian Technical Report of Fisheries and Aquatic Sciences, St. John’s, Newfoundland, p. 172Google Scholar
  45. Wang J (2004) Sibship reconstruction from genetic data with typing errors. Genet Soc Am 1979:1963–1979Google Scholar
  46. Wang J (2016) A comparison of single-sample estimators of effective population sizes from genetic marker data. Mol Ecol 25:4692–4711CrossRefPubMedGoogle Scholar
  47. Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352CrossRefPubMedGoogle Scholar
  48. Waples RS, Antao T (2014) Intermittent breeding and constraints on litter size: consequences for effective population size per generation (Ne) and per reproductive cycle (Nb). Evol Int J Org Evol 68:1722–1734CrossRefGoogle Scholar
  49. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756CrossRefPubMedGoogle Scholar
  50. 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 3:244–262CrossRefPubMedGoogle Scholar
  51. Waples RS, England PR (2011) Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 189:633–644CrossRefPubMedPubMedCentralGoogle Scholar
  52. Waples RS, Waples RS (2016) Making sense of genetic estimates of effective population size. Mol Ecol 25:4690–4691CrossRefGoogle Scholar
  53. Waples RS, Luikart G, Faulkner JR, Tallmon DA (2013) Simple life-history traits explain key effective population size ratios across diverse taxa. Proc R Soc Lond B 280:20131339CrossRefGoogle Scholar
  54. Waples RS, Antao T, Luikart G (2014) Effects of overlapping generations on linkage disequilibrium estimates of effective population size. Genetics 197:769–780CrossRefPubMedPubMedCentralGoogle Scholar
  55. Whiteley AR, Coombs JA, Hudy M et al (2013) Fragmentation and patch size shape genetic structure of brook trout populations. Can J Fish Aquatic Sci 688:678–688CrossRefGoogle Scholar
  56. Whiteley AR, Coombs JA, Cembrola M et al (2015) Effective number of breeders provides a link between interannual variation in stream flow and individual reproductive contribution in a stream salmonid. Mol Ecol 24:3585–3602CrossRefPubMedGoogle Scholar
  57. Whiteley AR, Coombs JA, Donnell MJO, Nislow KH, Letcher BH (2017) Keeping things local: subpopulation Nb and Ne in a stream network with partial barriers to fish migration. Evol Appl 348–365Google Scholar
  58. Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genet Soc Am 1191:1177–1191Google Scholar
  59. Wood JLA, Belmar-Lucero S, Hutchings IJ, Fraser DJ (2014) Relationship of habitat variability to population size in a stream fish. Ecol Appl 24:1085–1100CrossRefPubMedGoogle Scholar
  60. Wood JLA, Yates MC, Fraser DJ (2016) Are heritability and selection related to population size in nature? Meta-analysis and conservation implications. Evol Appl 9:640–657CrossRefPubMedPubMedCentralGoogle Scholar
  61. Yates M., Bernos TA, Fraser DJ (2017) A critical assessment of estimating census population size from genetic population size (or vice versa) in three fishes. Evol Appl. doi: 10.1111/eva.12496 PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  1. 1.Department of BiologyConcordia UniversityMontrealCanada

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