Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals.

Litzke V, Ottensmann M, Forcada J, Heitzmann L, Hoffman J (2019)
Ecology and evolution 9(14): 7985-7996.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
OA 1.08 MB
Litzke, Vivienne; Ottensmann, MeinolfUniBi; Forcada, Jaume; Heitzmann, Louise; Hoffman, JosephUniBi
Abstract / Bemerkung
Numerous studies have reported correlations between the heterozygosity of genetic markers and fitness. These heterozygosity-fitness correlations (HFCs) play a central role in evolutionary and conservation biology, yet their mechanistic basis remains open to debate. For example, fitness associations have been widely reported at both neutral and functional loci, yet few studies have directly compared the two, making it difficult to gauge the relative contributions of genome-wide inbreeding and specific functional genes to fitness. Here, we compared the effects of neutral and immune gene heterozygosity on death from bacterial infection in Antarctic fur seal (Arctocephalus gazella) pups. We specifically developed a panel of 13 microsatellites from expressed immune genes and genotyped these together with 48 neutral loci in 234 individuals, comprising 39 pups that were classified at necropsy as having most likely died of bacterial infection together with a five times larger matched sample of healthy surviving pups. Identity disequilibrium quantified from the neutral markers was positive and significant, indicative of variance in inbreeding within the study population. However, multilocus heterozygosity did not differ significantly between healthy and infected pups at either class of marker, and little evidence was found for fitness associations at individual loci. These results support a previous study of Antarctic fur seals that found no effects of heterozygosity at nine neutral microsatellites on neonatal survival and thereby help to refine our understanding of how HFCs vary across the life cycle. Given that nonsignificant HFCs are underreported in the literature, we also hope that our study will contribute toward a more balanced understanding of the wider importance of this phenomenon.
Ecology and evolution
Open-Access-Publikationskosten wurden durch die Universität Bielefeld im Rahmen des DEAL-Vertrags gefördert.
Page URI


Litzke V, Ottensmann M, Forcada J, Heitzmann L, Hoffman J. Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals. Ecology and evolution. 2019;9(14):7985-7996.
Litzke, V., Ottensmann, M., Forcada, J., Heitzmann, L., & Hoffman, J. (2019). Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals. Ecology and evolution, 9(14), 7985-7996. doi:10.1002/ece3.5317
Litzke, V., Ottensmann, M., Forcada, J., Heitzmann, L., and Hoffman, J. (2019). Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals. Ecology and evolution 9, 7985-7996.
Litzke, V., et al., 2019. Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals. Ecology and evolution, 9(14), p 7985-7996.
V. Litzke, et al., “Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals.”, Ecology and evolution, vol. 9, 2019, pp. 7985-7996.
Litzke, V., Ottensmann, M., Forcada, J., Heitzmann, L., Hoffman, J.: Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals. Ecology and evolution. 9, 7985-7996 (2019).
Litzke, Vivienne, Ottensmann, Meinolf, Forcada, Jaume, Heitzmann, Louise, and Hoffman, Joseph. “Heterozygosity at neutral and immune loci is not associated with neonatal mortality due to microbial infection in Antarctic fur seals.”. Ecology and evolution 9.14 (2019): 7985-7996.
Alle Dateien verfügbar unter der/den folgenden Lizenz(en):
Creative Commons Namensnennung 4.0 International Public License (CC-BY 4.0):
Access Level
OA Open Access
Zuletzt Hochgeladen
MD5 Prüfsumme

81 References

Daten bereitgestellt von Europe PubMed Central.

Genetic resistance to bovine tuberculosis in the Iberian wild boar.
Acevedo-Whitehouse K, Vicente J, Gortazar C, Hofle U, Fernandez-de-Mera IG, Amos W., Mol. Ecol. 14(10), 2005
PMID: 16101786
Contrasting effects of heterozygosity on survival and hookworm resistance in California sea lion pups.
Acevedo-Whitehouse K, Spraker TR, Lyons E, Melin SR, Gulland F, Delong RL, Amos W., Mol. Ecol. 15(7), 2006
PMID: 16689912
Long‐term preservation of whale skin for DNA analysis
MHC genotype and near-deterministic mortality in grey seals.
de Assuncao-Franco M, Hoffman JI, Harwood J, Amos W., Sci Rep 2(), 2012
PMID: 22997548
Does heterozygosity estimate inbreeding in real populations?
Balloux F, Amos W, Coulson T., Mol. Ecol. 13(10), 2004
PMID: 15367117
ADHD in DSM-5: a field trial in a large, representative sample of 18- to 19-year-old adults.
Matte B, Anselmi L, Salum GA, Kieling C, Goncalves H, Menezes A, Grevet EH, Rohde LA., Psychol Med 45(2), 2014
PMID: 25066615
Patterns of parental relatedness and pup survival in the grey seal (Halichoerus grypus).
Bean K, Amos W, Pomeroy PP, Twiss SD, Coulson TN, Boyd IL., Mol. Ecol. 13(8), 2004
PMID: 15245408
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Correlations between fitness and heterozygosity at allozyme and microsatellite loci in the Atlantic salmon, Salmo salar L.
Borrell YJ, Pineda H, McCarthy I, Vazquez E, Sanchez JA, Lizana GB., Heredity (Edinb) 92(6), 2004
PMID: 15162118
Scan of human genome reveals no new Loci under ancient balancing selection.
Bubb KL, Bovee D, Buckley D, Haugen E, Kibukawa M, Paddock M, Palmieri A, Subramanian S, Zhou Y, Kaul R, Green P, Olson MV., Genetics 173(4), 2006
PMID: 16751668
Multimodel inference: Understanding AIC and BIC in Model Selection
A quantitative review of heterozygosity-fitness correlations in animal populations.
Chapman JR, Nakagawa S, Coltman DW, Slate J, Sheldon BC., Mol. Ecol. 18(13), 2009
PMID: 19500255
The genetic basis of inbreeding depression.
Charlesworth B, Charlesworth D., Genet. Res. 74(3), 1999
PMID: 10689809
The genetics of inbreeding depression.
Charlesworth D, Willis JH., Nat. Rev. Genet. 10(11), 2009
PMID: 19834483
Confidence intervals are a more useful complement to nonsignificant tests than are power calculations
Coltman DW, Pilkington JG, Smith JA, Pemberton JM., Evolution 53(4), 1999
PMID: 28565537
Microsatellite measures of inbreeding: a meta-analysis.
Coltman DW, Slate J., Evolution 57(5), 2003
PMID: 12836816
Heterozygosity-fitness correlations revealed by neutral and candidate gene markers in roe deer from a long-term study.
Da Silva A, Gaillard JM, Yoccoz NG, Hewison AJ, Galan M, Coulson T, Allaine D, Vial L, Delorme D, Van Laere G, Klein F, Luikart G., Evolution 63(2), 2008
PMID: 19154375
Correlates with body size and mass in yearling brown bears (Ursus arctos)
Heterozygosity-fitness correlations: new perspectives on old problems.
David P., Heredity (Edinb) 80 ( Pt 5)(), 1998
PMID: 9650277
Reliable selfing rate estimates from imperfect population genetic data.
David P, Pujol B, Viard F, Castella V, Goudet J., Mol. Ecol. 16(12), 2007
PMID: 17561907
Density‐dependent pup mortality in the Antarctic fur seal Arctocephalus gazellu at South Georgia
Male contest competition and the coevolution of weaponry and testes in pinnipeds.
Fitzpatrick JL, Almbro M, Gonzalez-Voyer A, Kolm N, Simmons LW., Evolution 66(11), 2012
PMID: 23106721
Heterozygosity-fitness correlations in zebra finches: microsatellite markers can be better than their reputation.
Forstmeier W, Schielzeth H, Mueller JC, Ellegren H, Kempenaers B., Mol. Ecol. 21(13), 2012
PMID: 22554318
On the correlation between heterozygosity and fitness in natural populations.
Hansson B, Westerberg L., Mol. Ecol. 11(12), 2002
PMID: 12453232
Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches.
Hawley DM, Sydenstricker KV, Kollias GV, Dhondt AA., Biol. Lett. 1(3), 2005
PMID: 17148199
Is there a genetic basis for antler and pedicle malformations in reintroduced Elk in Northern Arizona?
The Abuse of Power
Female fur seals show active choice for males that are heterozygous and unrelated.
Hoffman JI, Forcada J, Trathan PN, Amos W., Nature 445(7130), 2007
PMID: 17287726
High-throughput sequencing reveals inbreeding depression in a natural population.
Hoffman JI, Simpson F, David P, Rijks JM, Kuiken T, Thorne MA, Lacy RC, Dasmahapatra KK., Proc. Natl. Acad. Sci. U.S.A. 111(10), 2014
PMID: 24586051
Extreme natal philopatry in female Antarctic fur seals (Arctocephalus gazella)
A novel approach for mining polymorphic microsatellite markers in silico.
Hoffman JI, Nichols HJ., PLoS ONE 6(8), 2011
PMID: 21853104
RAD Sequencing and a Hybrid Antarctic Fur Seal Genome Assembly Reveal Rapidly Decaying Linkage Disequilibrium, Global Population Structure and Evidence for Inbreeding.
Humble E, Dasmahapatra KK, Martinez-Barrio A, Gregorio I, Forcada J, Polikeit AC, Goldsworthy SD, Goebel ME, Kalinowski J, Wolf JBW, Hoffman JI., G3 (Bethesda) 8(8), 2018
PMID: 29954843
Global threats to pinnipeds
Balancing claims for balancing selection.
Kreitman M, Di Rienzo A., Trends Genet. 20(7), 2004
PMID: 15219394
Disentangling the contribution of sexual selection and ecology to the evolution of size dimorphism in pinnipeds.
Kruger O, Wolf JB, Jonker RM, Hoffman JI, Trillmich F., Evolution 68(5), 2014
PMID: 24475921
Heterozygosity-fitness correlations of conserved microsatellite markers in Kentish plovers Charadrius alexandrinus.
Kupper C, Kosztolanyi A, Augustin J, Dawson DA, Burke T, Szekely T., Mol. Ecol. 19(23), 2010
PMID: 21044191
Post hoc power analysis: an idea whose time has passed?
Levine M, Ensom MH., Pharmacotherapy 21(4), 2001
PMID: 11310512
Microsatellites: genomic distribution, putative functions and mutational mechanisms: a review.
Li YC, Korol AB, Fahima T, Beiles A, Nevo E., Mol. Ecol. 11(12), 2002
PMID: 12453231
Microsatellites within genes: structure, function, and evolution.
Li YC, Korol AB, Fahima T, Nevo E., Mol. Biol. Evol. 21(6), 2004
PMID: 14963101
Candidate gene microsatellite variation is associated with parasitism in wild bighorn sheep.
Luikart G, Pilgrim K, Visty J, Ezenwa VO, Schwartz MK., Biol. Lett. 4(2), 2008
PMID: 18270161
Effects of maternal age and condition on parturition and the perinatal period of Antarctic fur seals
Homozygosity and risk of childhood death due to invasive bacterial disease.
Lyons EJ, Amos W, Berkley JA, Mwangi I, Shafi M, Williams TN, Newton CR, Peshu N, Marsh K, Scott JA, Hill AV., BMC Med. Genet. 10(), 2009
PMID: 19523202

Effect size, confidence interval and statistical significance: a practical guide for biologists.
Nakagawa S, Cuthill IC., Biol Rev Camb Philos Soc 82(4), 2007
PMID: 17944619

Heterozygosity and lungworm burden in harbour seals (Phoca vitulina).
Rijks JM, Hoffman JI, Kuiken T, Osterhaus AD, Amos W., Heredity (Edinb) 100(6), 2008
PMID: 18398424

An economic method for the fluorescent labeling of PCR fragments.
Schuelke M., Nat. Biotechnol. 18(2), 2000
PMID: 10657137
The rate and spectrum of microsatellite mutation in Caenorhabditis elegans and Daphnia pulex.
Seyfert AL, Cristescu ME, Frisse L, Schaack S, Thomas WK, Lynch M., Genetics 178(4), 2008
PMID: 18430937
Statistical power analysis in wildlife research
Chemical fingerprints encode mother-offspring similarity, colony membership, relatedness, and genetic quality in fur seals.
Stoffel MA, Caspers BA, Forcada J, Giannakara A, Baier M, Eberhart-Phillips L, Muller C, Hoffman JI., Proc. Natl. Acad. Sci. U.S.A. 112(36), 2015
PMID: 26261311
inbreedR: an R package for the analysis of inbreeding based on genetic markers
Demographic histories and genetic diversity across pinnipeds are shaped by human exploitation, ecology and life-history.
Stoffel MA, Humble E, Paijmans AJ, Acevedo-Whitehouse K, Chilvers BL, Dickerson B, Galimberti F, Gemmell NJ, Goldsworthy SD, Nichols HJ, Kruger O, Negro S, Osborne A, Pastor T, Robertson BC, Sanvito S, Schultz JK, Shafer ABA, Wolf JBW, Hoffman JI., Nat Commun 9(1), 2018
PMID: 30446730
Heterozygosity-fitness correlations: a time for reappraisal.
Szulkin M, Bierne N, David P., Evolution 64(5), 2010
PMID: 20148954
Inbreeding coefficient and heterozygosity-fitness correlations in unhatched and hatched song sparrow nestmates.
Taylor SS, Sardell RJ, Reid JM, Bucher T, Taylor NG, Arcese P, Keller LF., Mol. Ecol. 19(20), 2010
PMID: 20854411

Primer3Plus, an enhanced web interface to Primer3.
Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JA., Nucleic Acids Res. 35(Web Server issue), 2007
PMID: 17485472
Reduced microsatellite heterozygosity does not affect natal dispersal in three contrasting roe deer populations.
Vanpe C, Debeffe L, Hewison AJM, Quemere E, Lemaitre JF, Galan M, Amblard B, Klein F, Cargnelutti B, Capron G, Merlet J, Warnant C, Gaillard JM., Oecologia 177(3), 2014
PMID: 25388875
No correlation between neonatal fitness and heterozygosity in a reintroduced population of Père David's deer


Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®


PMID: 31380066
PubMed | Europe PMC

Suchen in

Google Scholar