Abstract
Although hybridization can be used as a tool for genetic rescue, it can also generate outbreeding depression and reduce local adaptation. Improved understanding of these processes is required to better inform conservation decisions for threatened populations. Few studies, however, investigate how multiple factors influence hybridization effects. We investigated how effective population sizes (Ne), geographic distance, genetic divergence (QST, FST), and environmental stress influence hybridization effects among eight highly divergent brook trout (Salvelinus fontinalis) populations varying in Ne (range 44–589). In a common garden, we compared three fitness-related traits among hybrid and non-hybrid crosses. Contrary to expectations, we found little evidence of outbreeding depression; instead, hybridization effects were mostly neutral (60/66 non-hybrid vs. hybrid comparisons) with some support for heterosis (6/66). When controlling for maternal-family effects, several factors influenced fitness-related traits but cumulatively explained little variance in relative hybrid fitness (0–6.4%). For instance, when hybridized dams came from small Ne populations, relative fitness increased for some traits (length at hatch), suggesting heterosis, yet decreased at other traits (survival to hatch), suggesting outbreeding depression. Trait inconsistencies in relative hybrid fitness were also observed under different degrees of environmental stress. Results also differed when family variance in hybridization effects was unaccounted for. Collectively, our results suggest that, under certain conditions, current guidelines on genetic rescue and associated outbreeding risks might be too conservative. The occurrence of genetic rescue and outbreeding depression, nonetheless, remain difficult to predict because families and individual traits can express different effects from hybridization within populations.
Similar content being viewed by others
References
Araki H, Cooper B, Blouin MS (2007) Genetic effects of captive breeding cause a rapid, cumulative fitness decline in the wild. Science 318:100–103. https://doi.org/10.1126/science.1145621
Araki H, Berejikian BA, Ford MJ, Blouin MS (2008) Fitness of hatchery-reared salmonids in the wild. Evol Appl 1:342–355. https://doi.org/10.1111/j.1752-4571.2008.00026.x
Baker JP, Van Sickle J, Gagen CJ et al (1996) Episodic acidification of small streams in the northeastern united states: effects on fish populations. Ecol Appl 6:422–437. https://doi.org/10.2307/2269380
Bashey F (2008) Competition as a selective mechanism for larger offspring size in guppies. Oikos 117:104–113. https://doi.org/10.1111/j.2007.0030-1299.16094.x
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw. https://doi.org/10.18637/jss.v067.i01
Beacham TD, Murray CB (1985) Effect of female size, egg size, and water temperature on developmental biology of chum salmon (< i>Oncorhynchus keta < i>) from the Nitinat River, British Columbia. Can J Fish Aquat Sci 42:1755–1765. https://doi.org/10.1139/f85-220
Bernos TA, Fraser DJ (2016) Spatiotemporal relationship between adult census size and genetic population size across a wide population size gradient. Mol Ecol 25:4472–4487. https://doi.org/10.1111/mec.13790
Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796. https://doi.org/10.1038/nrg2664
Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56(12):2347–2358
Danzmann RG, Morgan RP II, Jones MW et al (1998) A major sextet of mitochondrial DNA phylogenetic assemblages extant in eastern North American brook trout (Salvelinus fontinalis): distribution and postglacial dispersal patterns. Can J Zool 76:1300–1318. https://doi.org/10.1139/cjz-76-7-1300
Debes PV, Fraser DJ, McBride MC, Hutchings JA (2013) Multigenerational hybridisation and its consequences for maternal effects in Atlantic salmon. Heredity (Edinb) 111:238–247. https://doi.org/10.1038/hdy.2013.43
Debes PV, Fraser DJ, Yates M, Hutchings JA (2014) The between-population genetic architecture of growth, maturation, and plasticity in Atlantic Salmon. Genetics 196(4):1277–1291. https://doi.org/10.1534/genetics.114.161729
Edmands S (1999) Heterosis and outbreeding depression in interpopulation crosses spanning a wide range of divergence. Evolution (N Y) 53:1757–1768. https://doi.org/10.2307/2640438
Edmands S (2002) Does parental divergence predict reproductive compatibility? Trends Ecol Evol 17:520–527
Edmands S (2007) Between a rock and a hard place: evaluating the relative risks of inbreeding and outbreeding for conservation and management. Mol Ecol 16:463–475
Edmands S, Deimler JK (2004) Local adaptation, intrinsic coadaptation and the effects of environmental stress on interpopulation hybrids in the copepod Tigriopus californicus. J Exp Mar Bio Ecol 303:183–196. https://doi.org/10.1016/j.jembe.2003.11.012
Einum S, Fleming IA (2000) Selection against late emergence and small offspring in Atlantic salmon (Salmo salar). Evolution (N Y) 54:628–639. https://doi.org/10.1111/j.0014-3820.2000.tb00064.x
Flebbe PA, Roghair LD, Bruggink JL (2006) Spatial modeling to project Southern Appalachian trout distribution in a warmer climate. Trans Am Fish Soc 135:1371–1382. https://doi.org/10.1577/T05-217.1
Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927. https://doi.org/10.1016/J.BIOCON.2010.05.011
Frankham R (2015) Genetic rescue of small inbred populations: meta-analysis reveals large and consistent benefits of gene flow. Mol Ecol 24:2610–2618. https://doi.org/10.1111/mec.13139
Frankham R, Briscoe DA, Ballou JD (2002) Introduction to conservation genetics. Cambridge University Press, Cambridge
Frankham R, Ballou JD, Eldridge MDB et al (2011) Predicting the probability of outbreeding depression. Conserv Biol 25:465–475. https://doi.org/10.1111/j.1523-1739.2011.01662.x
Frankham R, Brook BW, Bradshaw CJA, Traill LW, Spielman D (2013) 50/500 rule and minimum viable populations: response to Jamieson and Allendorf. Trends in Ecol Evol 28(4):187–188. https://doi.org/10.1016/j.tree.2013.01.002
Frankham R, Bradshaw CJA, Brook BW (2014) Genetics in conservation management: revised recommendations for the 50/500 rules, Red List criteria and population viability analyses. Biol Conserv 170:56–63. https://doi.org/10.1016/j.biocon.2013.12.036
Fraser DJ, Cook AM, Eddington JD, Bentzen P, Hutchings JA (2008) Mixed evidence for reduced local adaptation in wild salmon resulting from interbreeding with escaped farmed salmon: complexities in hybrid fitness. Evol Appl 1:501–512. https://doi.org/10.1111/j.1752-4571.2008.00037.x
Fraser DJ, Houde ALS, Debes PV et al (2010) Consequences of farmed-wild hybridization across divergent wild populations and multiple traits in salmon. Ecol Appl 20:935–953. https://doi.org/10.1890/09-0694.1
Fraser DJ, Weir LK, Bernatchez L et al (2011) Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity (Edinb) 106:404–420. https://doi.org/10.1038/hdy.2010.167
Fraser DJ, Debes PV, Bernatchez L, Hutchings JA (2014) Population size, habitat fragmentation, and the nature of adaptive variation in a stream fish. Proc R Soc B Biol Sci 281:8. https://doi.org/10.1098/rspb.2014.0370
Fraser DJ, Walker L, Yates MC, et al (2019) Population correlates of rapid captive-induced maladaptation in a wild fish. Evol Appl. https://doi.org/10.1111/eva.12649
Gilk SE, Wang IA, Hoover CL et al (2004) Outbreeding depression in hybrids between spatially separated Pink Salmon, Oncorhynchus gorbuscha, populations: marine survival, homing ability, and variability in family size. Environ Biol Fishes 69:287–297. https://doi.org/10.1023/B:EBFI.0000022888.28218.c1
Grindeland JM (2008) Inbreeding depression and outbreeding depression in Digitalis purpurea: optimal outcrossing distance in a tetraploid. J Evol Biol 21:716–726. https://doi.org/10.1111/j.1420-9101.2008.01519.x
Hijmans R, Williams E, Vennes C, Hijmans M (2015) Package “geosphere”
Houde ALS, Fraser DJ, Hutchings JA (2010) Fitness-related consequences of competitive interactions between farmed and wild Atlantic salmon at different proportional representations of wild-farmed hybrids. ICES J Mar Sci 67:657–667. https://doi.org/10.1093/icesjms/fsp272
Houde ALS, Fraser DJ, O’Reilly P, Hutchings JA (2011) Relative risks of inbreeding and outbreeding depression in the wild in endangered salmon. Evol Appl 4:634–647. https://doi.org/10.1111/j.1752-4571.2011.00186.x
Hudy M, Thieling TM, Gillespie N, Smith EP (2008) Distribution, status, and land use characteristics of Subwatersheds within the native range of brook trout in the Eastern United States. North Am J Fish Manag 28:1069–1085. https://doi.org/10.1577/M07-017.1
Husband BC, Schemske DW (1997) The effect of inbreeding in diploid and tetraploid populations of Epilobium angustifolium (Onagraceae): implications for the genetic basis of inbreeding depression. Evolution (N Y) 51:737–746. https://doi.org/10.2307/2411150
Huss M, Byström P, Strand Å et al (2008) Influence of growth history on the accumulation of energy reserves and winter mortality in young fish. Can J Fish Aquat Sci 65:2149–2156. https://doi.org/10.1139/F08-115
Hutchings JA (1996) Adaptive phenotypic plasticity in brook trout, Salvelinus fontinalis, life histories. Écoscience 3:25–32. https://doi.org/10.1080/11956860.1996.11682311
Kanno Y, Vokoun JC, Letcher BH (2011) Sibship reconstruction for inferring mating systems, dispersal and effective population size in headwater brook trout (Salvelinus fontinalis) populations. Conserv Genet 12:619–628. https://doi.org/10.1007/s10592-010-0166-9
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. https://doi.org/10.1016/S0169-5347(02)02489-8
Kelly JK (2005) Family level inbreeding depression and the evolution of plant mating systems. New Phytol 165(1):55–62
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53(3):983. https://doi.org/10.2307/2533558
Kronenberger JA, Funk WC, Smith JW et al (2017) Testing the demographic effects of divergent immigrants on small populations of Trinidadian guppies. Anim Conserv 20:3–11. https://doi.org/10.1111/acv.12286
Leberg PL, Firmin BD (2008) Role of inbreeding depression and purging in captive breeding and restoration programmes. Mol Ecol 17(1):334–343. https://doi.org/10.1111/j.1365-294X.2007.03433.x
Leinonen T, McCairns RJS, O’Hara RB, Merilä J (2013) QST–FST comparisons: evolutionary and ecological insights from genomic heterogeneity. Nat Rev Genet 14:179–190. https://doi.org/10.1038/nrg3395
Lemmon EM, Juenger TE (2017) Geographic variation in hybridization across a reinforcement contact zone of chorus frogs (Pseudacris). Ecol Evol 7:9485–9502. https://doi.org/10.1002/ece3.3443
Lynch M (1991) The genetic interpretation of inbreeding depression and outbreeding depression. Evolution (N Y) 45:622–629. https://doi.org/10.2307/2409915
Marten PS (1992) Effect of temperature variation on the incubation and development of brook trout eggs. Progress Fish-Culturist 54:1–6
Mavárez J, Salazar CA, Bermingham E et al (2006) Speciation by hybridization in Heliconius butterflies. Nature 441:868–871. https://doi.org/10.1038/nature04738
McClelland EK, Naish KA (2007) What is the fitness outcome of crossing unrelated fish populations? A meta-analysis and an evaluation of future research directions. Conserv Genet 8:397–416. https://doi.org/10.1007/s10592-006-9178-x
Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R 2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142. https://doi.org/10.1111/j.2041-210x.2012.00261.x
Oehlert GW (1992) A note on the delta method. Am Stat 46:27–29. https://doi.org/10.1080/00031305.1992.10475842
Pess GR, Kiffney PM, Liermann MC et al (2011) The influences of body size, habitat quality, and competition on the movement and survival of juvenile coho salmon during the early stages of stream recolonization. Trans Am Fish Soc 140:883–897. https://doi.org/10.1080/00028487.2011.587752
Pickup M, Young AG (2008) Population size, self-incompatibility and genetic rescue in diploid and tetraploid races of Rutidosis leptorrhynchoides (Asteraceae). Heredity (Edinb) 100:268–274. https://doi.org/10.1038/sj.hdy.6801070
Pickup M, Field DL, Rowell DM, Young AG (2013) Source population characteristics affect heterosis following genetic rescue of fragmented plant populations. Proc R Soc B Biol Sci 280:20122058. https://doi.org/10.1098/rspb.2012.2058
Pierce AA, Gutierrez R, Rice AM, Pfennig KS (2017) Genetic variation during range expansion: effects of habitat novelty and hybridization. Proc Biol Sci 284:20170007. https://doi.org/10.1098/rspb.2017.0007
Prill N, Bullock JM, van Dam NM, Leimu R (2014) Loss of heterosis and family-dependent inbreeding depression in plant performance and resistance against multiple herbivores under drought stress. J Ecol 102:1497–1505. https://doi.org/10.1111/1365-2745.12327
Quinn TP, Peterson NP (1996) The influence of habitat complexity and fish size on over-winter survival and growth of individually marked juvenile coho salmon (Oncorhynchus kisutch) in Big Beef Creek, Washington. Can J Fish Aquat Sci 53:1555–1564. https://doi.org/10.1139/f96-092
R Development Core Team (2008) R: a language and environment for statistical computing. R Core Team, Vienna
Ralls K, Ballou JD, Dudash MR et al (2017) Call for a Paradigm Shift in the genetic management of fragmented populations. Conserv Lett 11:e12412. https://doi.org/10.1111/conl.12412
Ramachandran S, Deshpande O, Roseman CC et al (2005) Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa. Proc Natl Acad Sci USA 102:15942–15947. https://doi.org/10.1073/pnas.0507611102
Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237. https://doi.org/10.1046/j.1523-1739.2003.01236.x
Robinson ZL, Coombs JA, Hudy M et al (2017) Experimental test of genetic rescue in isolated populations of brook trout. Mol Ecol 26:4418–4433. https://doi.org/10.1111/mec.14225
Stabell OB (1984) Homing and olfaction in salmonids: a critical review with special reference to the Atlantic Salmon. Biol Rev 59:333–388. https://doi.org/10.1111/j.1469-185X.1984.tb00709.x
Thorgaard GH, Allendorf FW, Knudsen KL (1983) Gene-centromere mapping in rainbow trout: high interference over long map distances. Genetics 103:771–783
Tallmon D, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. Trends Ecol Evol 19(9):489–496. https://doi.org/10.1016/j.tree.2004.07.003
Wells ZRR, McDonnell LH, Chapman LJ, Fraser DJ (2016) Limited variability in upper thermal tolerance among pure and hybrid populations of a cold-water fish. Conserv Physiol 4:cow063. https://doi.org/10.1093/conphys/cow063
Wenger SJ, Isaak DJ, Luce CH et al (2011) Flow regime, temperature, and biotic interactions drive differential declines of trout species under climate change. Proc Natl Acad Sci USA 108:14175–14180. https://doi.org/10.1073/pnas.1103097108
Whiteley AR, Fitzpatrick SW, Funk WC, Tallmon DA (2015) Genetic rescue to the rescue. Trends Ecol Evol 30:42–49. https://doi.org/10.1016/J.TREE.2014.10.009
Willett CS (2012) Hybrid breakdown weakens under thermal stress in population crosses of the copepod Tigriopus californicus. J Hered 103:103–114. https://doi.org/10.1093/jhered/esr109
Willi Y, Van Buskirk J, Hoffmann AA et al (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst Annu Rev Ecol Evol Syst 37:433–458. https://doi.org/10.2307/annurev.ecolsys.37.091305.30000017
Wood JLA, Fraser DJ (2015) Similar plastic responses to elevated temperature among differentially abundant brook trout populations. Ecology 96:1010–1019. https://doi.org/10.1890/14-1378.1
Wood JLA, Belmar-Lucero S, Hutchings JA, Fraser DJ (2014) Relationship of habitat variability to population size in a stream fish. Ecol Appl 24:1085–1100. https://doi.org/10.1890/13-1647.1
Wood JLA, Tezel D, Joyal D, Fraser DJ (2015) Population size is weakly related to quantitative genetic variation and trait differentiation in a stream fish. Evolution (N Y) 69:2303–2318. https://doi.org/10.1111/evo.12733
Zastavniouk C, Weir LK, Fraser DJ (2017) The evolutionary consequences of habitat fragmentation: body morphology and coloration differentiation among brook trout populations of varying size. Ecol Evol 7:6850–6862. https://doi.org/10.1002/ece3.3229
Acknowledgements
We thank DFO (Newfoundland) for providing permits to conduct field collections of brook trout gametes, J. Wood and C. Zastavniouk for assistance with gamete collections, and K. Marin and S. Islam for their assistance in gamete crossing and fish husbandry. This study was supported by NSERC Discovery and Accelerator Grants to D. Fraser and an NSERC Postgraduate Scholarship to M. Yates. Finally, we thank Dr. J.C. Garza and two anonymous reviewers for their valuable comments on a previous version of our manuscript.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Wells, Z.R.R., Bernos, T.A., Yates, M.C. et al. Genetic rescue insights from population- and family-level hybridization effects in brook trout. Conserv Genet 20, 851–863 (2019). https://doi.org/10.1007/s10592-019-01179-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-019-01179-z