Abstract
Inbreeding depression (ID) occurs when inbreeding negatively impacts fitness. Understanding ID in wildlife is crucial for conservation and management, but obtaining good estimates of inbreeding and fitness to study ID on such systems can be challenging. Furthermore, the possible modulation of ID by various intrinsic and extrinsic variables can make its detection and interpretation uncertain in the absence of detailed individual and environmental information. Here we tested for ID in the culturally important population of feral horses (Equus ferus caballus) of Sable Island, Canada, using inbreeding coefficients derived from ~ 30,000 Single Nucleotide Polymorphisms (SNPs) and individual-based data for three fitness-related traits (body condition [BC], strongyle fecal egg count [FEC], and age at first reproduction [AFR]). We further assessed whether the expression of ID in this population was modulated by intrinsic (age, sex, reproductive status) and extrinsic (location, year) variables. ID was detected for all traits but mediating variables differed. For both BC and FEC, ID varied among years and was greater in the western portion of the island. In contrast, ID for BC was strongest in juveniles and lactating mares while for FEC it was strongest for reproductive-aged horses and males. Lastly, ID for AFR was mediated by cohort effects. Our study indicates that ID is impacting the fitness and welfare of Sable Island horses, but that its intensity varies among traits and ecological contexts. This illustrates the importance of considering both intrinsic and extrinsic variables to understand the expression of ID in the wild.
Similar content being viewed by others
Data availability
The datasets generated and analysed during the current study are available from the corresponding author on reasonable request.
References
Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235–242. https://doi.org/10.1038/sj.hdy.6800721
Bartoń K (2013) MuMIn: Multi-model inference
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting Linear Mixed-Effects Models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Becher AM, Mahling M, Nielsen MK, Pfister K (2010) Selective anthelmintic therapy of horses in the Federal states of Bavaria (Germany) and Salzburg (Austria): an investigation into strongyle egg shedding consistency. Vet Parasitol 171:116–122. https://doi.org/10.1016/j.vetpar.2010.03.001
Becker PJJ, Hegelbach J, Keller LF, Postma E (2016) Phenotype-associated inbreeding biases estimates of inbreeding depression in a wild bird population. J Evol Biol 29:35–46. https://doi.org/10.1111/jeb.12759
Bérénos C, Ellis PA, Pilkington JG, Pemberton JM (2016) Genomic analysis reveals depression due to both individual and maternal inbreeding in a free-living mammal population. Mol Ecol 25:3152–3168. https://doi.org/10.1111/mec.13681
Biscarini F, Cozzi P, Gaspa G, Marras G (2018) detectRUNS: Detect runs of homozygosity and runs of heterozygosity in diploid genomes. https://cran.r-project.org/web/packages/detectRUNS/index.html. Accessed 29 Feb 2020
Blanchard RJ, McKittrick CR, Blanchard DC (2001) Animal models of social stress: effects on behavior and brain neurochemical systems. Physiol Behav 73:261–271. https://doi.org/10.1016/S0031-9384(01)00449-8
Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci 106:13850–13853. https://doi.org/10.1073/pnas.0900639106
Casellas J, Piedrafita J, Caja G, Varona L (2009) Analysis of founder-specific inbreeding depression on birth weight in Ripollesa lambs1. J Anim Sci 87:72–79. https://doi.org/10.2527/jas.2008-0897
Chang CC, Chow CC, Tellier LC et al (2015) Second-generation PLINK: rising to the challenge of larger and richer datasets. Gigascience 4:7. https://doi.org/10.1186/s13742-015-0047-8
Christie BJ (1995) The horses of Sable Island. Pottersfield Pr, Lawrencetown Beach, N.S
Colpitts J, McLoughlin PD, Poissant J (2022) Runs of homozygosity in Sable Island feral horses reveal the genomic consequences of inbreeding and divergence from domestic breeds. BMC Genomics 23:501. https://doi.org/10.1186/s12864-022-08729-9
Contasti AL, Beest FMV, Wal EV, Mcloughlin PD (2013) Identifying hidden sinks in growing populations from individual fates and movements: the feral horses of Sable Island. J Wildl Manag 77:1545–1552. https://doi.org/10.1002/jwmg.625
Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270. https://doi.org/10.1046/j.1365-2540.1999.00553.x
Davison AC, Hinkley DV (1997) Bootstrap methods and their application. Cambridge University Press, Cambridge
Debeffe L, Mcloughlin PD, Medill SA et al (2016) Negative covariance between parasite load and body condition in a population of feral horses. Parasitology 143:983–997. https://doi.org/10.1017/S0031182016000408
Debeffe L, Poissant J, McLoughlin PD (2017) Individual quality and age but not environmental or social conditions modulate costs of reproduction in a capital breeder. Ecol Evol 7:5580–5591. https://doi.org/10.1002/ece3.3082
Dunsmore JD (1965) Ostertagia spp. in lambs and pregnant ewes. J Helminthol 39:159–184. https://doi.org/10.1017/s0022149x00020575
Duntsch L, Whibley A, de Villemereuil P et al (2023) Genomic signatures of inbreeding depression for a threatened Aotearoa New Zealand passerine. Mol Ecol n/a. https://doi.org/10.1111/mec.16855
Ebel ER, Phillips PC (2016) Intrinsic differences between males and females determine sex-specific consequences of inbreeding. BMC Evol Biol 16:36. https://doi.org/10.1186/s12862-016-0604-5
Evans SR, Postma E, Sheldon BC (2020) It takes two: heritable male effects on reproductive timing but not clutch size in a wild bird population*. Evolution 74:2320–2331. https://doi.org/10.1111/evo.13980
Ferenčaković M, Sölkner J, Kapš M, Curik I (2017) Genome-wide mapping and estimation of inbreeding depression of semen quality traits in a cattle population. J Dairy Sci 100:4721–4730. https://doi.org/10.3168/jds.2016-12164
Fox J, Weisberg S (2019) An R companion to Applied Regression, 3rd edn. Sage Publications
Frankham R (2010) Inbreeding in the wild really does matter. Heredity 104:124–124. https://doi.org/10.1038/hdy.2009.155
Fritzen B, Rohn K, Schnieder T, Von Samson-Himmelstjerna G (2010) Endoparasite control management on horse farms – lessons from worm prevalence and questionnaire data. Equine Vet J 42:79–83. https://doi.org/10.2746/042516409X471485
Gold S, Regan CE, McLoughlin PD et al (2019) Quantitative genetics of gastrointestinal strongyle burden and associated body condition in feral horses. Int J Parasitology: Parasites Wildl 9:104–111. https://doi.org/10.1016/j.ijppaw.2019.03.010
Gómez MD, Valera M, Molina A et al (2009) Assessment of inbreeding depression for body measurements in spanish Purebred (andalusian) horses. Livest Sci 122:149–155. https://doi.org/10.1016/j.livsci.2008.08.007
Hayward AD, Wilson AJ, Pilkington JG et al (2009) Ageing in a variable habitat: environmental stress affects senescence in parasite resistance in St Kilda Soay sheep. Proc Royal Soc B: Biol Sci 276:3477–3485. https://doi.org/10.1098/rspb.2009.0906
Hayward AD, Behnke JM, Childs DZ et al (2022) Long-term temporal trends in gastrointestinal parasite infection in wild Soay sheep. Parasitology 149:1749–1759. https://doi.org/10.1017/S0031182022001263
Hedrick PW, Garcia-Dorado A (2016) Understanding Inbreeding Depression, purging, and genetic rescue. Trends Ecol Evol 31:940–952. https://doi.org/10.1016/j.tree.2016.09.005
Hedrick PW, Kalinowski ST (2000) Inbreeding depression in Conservation Biology. Annu Rev Ecol Syst 31:139–162. https://doi.org/10.1146/annurev.ecolsys.31.1.139
Huisman J, Kruuk LEB, Ellis PA et al (2016) Inbreeding depression across the lifespan in a wild mammal population. Proc Natl Acad Sci 113:3585–3590. https://doi.org/10.1073/pnas.1518046113
Kardos M, Luikart G, Allendorf FW (2015) Measuring individual inbreeding in the age of genomics: marker-based measures are better than pedigrees. Heredity 115:63–72. https://doi.org/10.1038/hdy.2015.17
Kardos M, Taylor HR, Ellegren H et al (2016) Genomics advances the study of inbreeding depression in the wild. Evol Appl 9:1205–1218. https://doi.org/10.1111/eva.12414
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
Keller LF, Grant PR, Grant BR, Petren K (2002) Environmental conditions affect the magnitude of Inbreeding Depression in Survival of Darwin’s finches. Evolution 56:1229–1239. https://doi.org/10.1111/j.0014-3820.2002.tb01434.x
Leroy G (2014) Inbreeding depression in livestock species: review and meta-analysis. Anim Genet 45:618–628. https://doi.org/10.1111/age.12178
Linklater WL, Cameron EZ, Minot EO, Stafford KJ (1999) Stallion harassment and the mating system of horses. Anim Behav 58:295–306. https://doi.org/10.1006/anbe.1999.1155
Marjamäki PH, Contasti AL, Coulson TN, McLoughlin PD (2013) Local density and group size interacts with age and sex to determine direction and rate of social dispersal in a polygynous mammal. Ecol Evol 3:3073–3082. https://doi.org/10.1002/ece3.694
Martikainen K, Koivula M, Uimari P (2020) Identification of runs of homozygosity affecting female fertility and milk production traits in finnish Ayrshire cattle. Sci Rep 10:3804. https://doi.org/10.1038/s41598-020-60830-9
Medill SA (1977) - (2018) Sociality of sable island horses: population, group, and individual interactions. Thesis, University of Saskatchewan
Nietlisbach P, Muff S, Reid JM et al (2019) Nonequivalent lethal equivalents: models and inbreeding metrics for unbiased estimation of inbreeding load. Evol Appl 12:266–279. https://doi.org/10.1111/eva.12713
Norén K, Godoy E, Dalén L et al (2016) Inbreeding depression in a critically endangered carnivore. Mol Ecol 25:3309–3318. https://doi.org/10.1111/mec.13674
Ott TL (2020) Immunological detection of pregnancy: evidence for systemic immune modulation during early pregnancy in ruminants. Theriogenology 150:498–503. https://doi.org/10.1016/j.theriogenology.2020.04.010
Pemberton JM, Ellis PE, Pilkington JG, Bérénos C (2017) Inbreeding depression by environment interactions in a free-living mammal population. Heredity 118:64–77. https://doi.org/10.1038/hdy.2016.100
Pepke ML, Niskanen AK, Kvalnes T et al (2022) Inbreeding is associated with shorter early-life telomere length in a wild passerine. Conserv Genet 23:639–651. https://doi.org/10.1007/s10592-022-01441-x
Plante Y, Vega-Pla JL, Lucas Z et al (2007) Genetic diversity in a feral Horse Population from Sable Island, Canada. J Hered 98:594–602. https://doi.org/10.1093/jhered/esm064
Poissant J, Gavriliuc S, Bellaw J et al (2021) A repeatable and quantitative DNA metabarcoding assay to characterize mixed strongyle infections in horses. Int J Parasitol 51:183–192. https://doi.org/10.1016/j.ijpara.2020.09.003
Primmer CR (2009) From Conservation Genetics to Conservation Genomics. Ann N Y Acad Sci 1162:357–368. https://doi.org/10.1111/j.1749-6632.2009.04444.x
Prystupa JM, Juras R, Cothran EG et al (2012) Genetic diversity and admixture among canadian, Mountain and Moorland and nordic pony populations. animal 6:19–30. https://doi.org/10.1017/S1751731111001212
R Core Team (2022) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ralls K, Ballou JD, Templeton A (1988) Estimates of Lethal Equivalents and the cost of inbreeding in mammals. Conserv Biol 2:185–193. https://doi.org/10.1111/j.1523-1739.1988.tb00169.x
Regan CE, Medill SA, Poissant J, McLoughlin PD (2020) Causes and consequences of an unusually male-biased adult sex ratio in an unmanaged feral horse population. J Anim Ecol 89:2909–2921. https://doi.org/10.1111/1365-2656.13349
Reid JM, Arcese P, Sardell RJ, Keller LF (2011) Additive genetic variance, heritability, and Inbreeding Depression in Male Extra-Pair Reproductive Success. Am Nat 177:177–187. https://doi.org/10.1086/657977
Richardson DS, Komdeur J, Burke T (2004) Inbreeding in the the Seychelles warbler: environment-dependent maternal effects. Evolution 58:2037–2048. https://doi.org/10.1111/j.0014-3820.2004.tb00488.x
Rozen-Rechels D, van Beest FM, Richard E et al (2015) Density-dependent, central-place foraging in a grazing herbivore: competition and tradeoffs in time allocation near water. Oikos 124:1142–1150. https://doi.org/10.1111/oik.02207
Saura M, Fernández A, Varona L et al (2015) Detecting inbreeding depression for reproductive traits in Iberian pigs using genome-wide data. Genet Sel Evol 47:1. https://doi.org/10.1186/s12711-014-0081-5
Steuer AE, Anderson HP, Shepherd T et al (2022) Parasite dynamics in untreated horses through one calendar year. Parasites & Vectors 15:50. https://doi.org/10.1186/s13071-022-05168-z
Stoffel MA, Johnston SE, Pilkington JG, Pemberton JM (2021) Genetic architecture and lifetime dynamics of inbreeding depression in a wild mammal. Nat Commun 12:2972. https://doi.org/10.1038/s41467-021-23222-9
Sumreddee P, Toghiani S, Hay EH et al (2020) Runs of homozygosity and analysis of inbreeding depression. J Anim Sci 98. https://doi.org/10.1093/jas/skaa361
Thompson JR, Everett RW, Wolfe CW (2000) Effects of Inbreeding on Production and Survival in Jerseys. J Dairy Sci 83:2131–2138. https://doi.org/10.3168/jds.S0022-0302(00)75096-X
Tissier EJ, Mcloughlin PD, Sheard JW, Johnstone JF (2013) Distribution of vegetation along environmental gradients on Sable Island, Nova Scotia. Écoscience 20:361–372. https://doi.org/10.2980/20-4-3616
Troianou E, Huisman J, Pemberton JM, Walling CA (2018) Estimating selection on the act of inbreeding in a population with strong inbreeding depression. J Evol Biol 31:1815–1827. https://doi.org/10.1111/jeb.13376
Ure D, McLoughlin PD, Frasier TR, Lucas Z (2016) Horse population status and trends, Sable Island National Park Reserve. Parks Canada Agency, Halifax, NS
Uzans AJ, Lucas Z, McLeod BA, Frasier TR (2015) Small ne of the isolated and unmanaged Horse Population on Sable Island. J Hered 106:660–665. https://doi.org/10.1093/jhered/esv051
Vega-Trejo R, de Boer RA, Fitzpatrick JL, Kotrschal A (2022) Sex-specific inbreeding depression: a meta-analysis. Ecol Lett 25:1009–1026. https://doi.org/10.1111/ele.13961
Wells DA, Cant MA, Nichols HJ, Hoffman JI (2018) A high-quality pedigree and genetic markers both reveal inbreeding depression for quality but not survival in a cooperative mammal. Mol Ecol 27:2271–2288. https://doi.org/10.1111/mec.14570
Welsh D (1975) Population, behavioural, and grazing ecology of the horses of Sable Island, Nova Scotia. Dalhousie University
White KL, Eason DK, Jamieson IG, Robertson BC (2015) Evidence of inbreeding depression in the critically endangered parrot, the kakapo. Anim Conserv 18:341–347. https://doi.org/10.1111/acv.12177
Yengo L, Zhu Z, Wray NR et al (2017) Detection and quantification of inbreeding depression for complex traits from SNP data. Proc Natl Acad Sci USA 114:8602–8607. https://doi.org/10.1073/pnas.1621096114
Acknowledgements
The authors would like to thank the past and present members of the Sable Island field crew for their tireless efforts collecting data each summer. Special thanks also to Drs. Lucie Debeffe and Charlotte Regan for generating body condition scores, Dr. Charlotte Regan for her help with coding and model selection theory, and to Dr. Pirmin Nietlisbach for his assistance with the estimation of inbreeding loads.
Funding
This work was supported by the Natural Sciences and Engineering Research Council of Canada (Discovery Grants Nos 2016–06459 to PDM and 2019–04388 to JP, and Vanier Canada Graduate Scholarship to JC), the Canada Foundation for Innovation (Leaders Opportunity Grant No 25046 to PDM), a Leverhulme Trust Early Career Fellowship (ECF-2014-564 to JP), and the University of Calgary.
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by JC and JP. The first draft of the manuscript was written by JC and all authors commented on previous versions of the manuscript. All authors have read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Ethics approval
All sampling, parasitology work, and genotyping was carried out under University of Saskatchewan Animal Care Protocol 20090032, University of Calgary Animal Care Protocol AC18-0078, and research permits granted by Parks Canada (SINP-2017-24036 and SINP-2021-38998). Researchers had express permission to enter Sable Island National Park Reserve to observe horses and collect samples in accordance with the Parks Canada wildlife interaction guidelines, the Canada Shipping Act and granted research permits. This study is reported in accordance with ARRIVE guidelines.
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
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Colpitts, J., McLoughlin, P.D. & Poissant, J. Inbreeding depression in Sable Island feral horses is mediated by intrinsic and extrinsic variables. Conserv Genet 25, 1–15 (2024). https://doi.org/10.1007/s10592-023-01549-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-023-01549-8