MHC-associated mate choice under competitive conditions in captive versus wild Tasmanian devils

Mate choice contributes to driving evolutionary processes when animals choose breeding partners that confer genetic advantages to offspring, such as increased immunocompetence. The major histocompatibility complex (MHC) is an important group of immunological molecules, as MHC antigens bind and present foreign peptides to T-cells. Recent studies suggest that mates may be selected based on their MHC profile, leading to an association between an individual’s MHC diversity and their breeding success. In conservation, it may be important to consider mate choice in captive breeding programs, as this mechanism may improve reproductive rates. We investigated the reproductive success of Tasmanian devils in a group housing facility to determine whether increased MHC-based heterozygosity led individuals to secure more mating partners and produce more offspring. We also compared the breeding success of captive females to a wild devil population. MHC diversity was quantified using 12 MHC-linked microsatellite markers, including 11 previously characterized markers and one newly identified marker. Our analyses revealed that there was no relationship between MHC-linked heterozygosity and reproductive success either in captivity or the wild. The results of this study suggest that, for Tasmanian devils, MHC-based heterozygosity does not produce greater breeding success and that no specific changes to current captive management strategies are required with respect to preserving MHC diversity.

[1]  C. Grueber,et al.  A Tasmanian devil breeding program to support wild recovery. , 2019, Reproduction, fertility, and development.

[2]  Parice A. Brandies,et al.  Disentangling the mechanisms of mate choice in a captive koala population , 2018, PeerJ.

[3]  Menna E. Jones,et al.  Density trends and demographic signals uncover the long-term impact of transmissible cancer in Tasmanian devils. , 2018, The Journal of applied ecology.

[4]  C. Grueber,et al.  Are any populations ‘safe’? Unexpected reproductive decline in a population of Tasmanian devils free of devil facial tumour disease , 2018, Wildlife Research.

[5]  C. Grueber,et al.  A meta-analysis of birth-origin effects on reproduction in diverse captive environments , 2018, Nature Communications.

[6]  Gregory P. Brown,et al.  MHC diversity and female age underpin reproductive success in an Australian icon; the Tasmanian Devil , 2018, Scientific Reports.

[7]  C. Grueber,et al.  The effects of group versus intensive housing on the retention of genetic diversity in insurance populations , 2018 .

[8]  R. Mulder,et al.  Opportunity for female mate choice improves reproductive outcomes in the conservation breeding program of the eastern barred bandicoot (Perameles gunnii) , 2017 .

[9]  C. Grueber,et al.  No evidence of inbreeding depression in a Tasmanian devil insurance population despite significant variation in inbreeding , 2017, Scientific Reports.

[10]  Menna E. Jones,et al.  Conservation implications of limited genetic diversity and population structure in Tasmanian devils (Sarcophilus harrisii) , 2017, Conservation Genetics.

[11]  E. Randi,et al.  Choosy Wolves? Heterozygote Advantage But No Evidence of MHC-Based Disassortative Mating. , 2016, The Journal of heredity.

[12]  A. B. Lyons,et al.  A second transmissible cancer in Tasmanian devils , 2015, Proceedings of the National Academy of Sciences.

[13]  He-min Zhang,et al.  Free mate choice enhances conservation breeding in the endangered giant panda , 2015, Nature Communications.

[14]  Wolfgang Forstmeier,et al.  Fitness Benefits of Mate Choice for Compatibility in a Socially Monogamous Species , 2015, PLoS biology.

[15]  Katherine Belov,et al.  Genomic insights into a contagious cancer in Tasmanian devils. , 2015, Trends in genetics : TIG.

[16]  C. Grueber,et al.  Lack of genetic diversity across diverse immune genes in an endangered mammal, the Tasmanian devil (Sarcophilus harrisii) , 2015, Molecular ecology.

[17]  N. Gemmell,et al.  Heterozygote advantage at MHC DRB may influence response to infectious disease epizootics , 2015, Molecular ecology.

[18]  J. Slate,et al.  No evidence for MHC class I‐based disassortative mating in a wild population of great tits , 2015, Journal of evolutionary biology.

[19]  P. Taberlet,et al.  No Evidence for the Effect of MHC on Male Mating Success in the Brown Bear , 2014, PloS one.

[20]  Shinichi Nakagawa,et al.  A quantitative review of MHC‐based mating preference: the role of diversity and dissimilarity , 2014, Molecular ecology.

[21]  G. Sorci,et al.  Can sexual selection theory inform genetic management of captive populations? A review , 2014, Evolutionary applications.

[22]  S. Altizer,et al.  Sexual selection explains more functional variation in the mammalian major histocompatibility complex than parasitism , 2013, Proceedings of the Royal Society B: Biological Sciences.

[23]  P. Kappeler,et al.  MHC‐disassortative mate choice and inbreeding avoidance in a solitary primate , 2013, Molecular ecology.

[24]  Menna E. Jones,et al.  Reversible epigenetic down-regulation of MHC molecules by devil facial tumour disease illustrates immune escape by a contagious cancer , 2013, Proceedings of the National Academy of Sciences.

[25]  J. Austin,et al.  Low major histocompatibility complex diversity in the Tasmanian devil predates European settlement and may explain susceptibility to disease epidemics , 2013, Biology Letters.

[26]  J. A. Clark,et al.  MHC diversity and mate choice in the magellanic penguin, Spheniscus magellanicus. , 2012, The Journal of heredity.

[27]  K. Belov,et al.  Isolation and characterisation of 11 MHC-linked microsatellite loci in the Tasmanian devil (Sarcophilus harrisii) , 2012, Conservation Genetics Resources.

[28]  Menna E. Jones,et al.  Low MHC class II diversity in the Tasmanian devil (Sarcophilus harrisii) , 2012, Immunogenetics.

[29]  R. Zenuto,et al.  Females prefer good genes: MHC-associated mate choice in wild and captive tuco-tucos , 2012, Animal Behaviour.

[30]  Carolyn Tregidgo,et al.  Genome Sequencing and Analysis of the Tasmanian Devil and Its Transmissible Cancer , 2012, Cell.

[31]  Mark R. Christie,et al.  Genetic adaptation to captivity can occur in a single generation , 2011, Proceedings of the National Academy of Sciences.

[32]  Tom H. Pringle,et al.  Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil) , 2011, Proceedings of the National Academy of Sciences.

[33]  I. Jamieson,et al.  Multimodel inference in ecology and evolution: challenges and solutions , 2011, Journal of evolutionary biology.

[34]  D. Penn,et al.  Female house sparrows "count on" male genes: experimental evidence for MHC-dependent mate preference in birds , 2011, BMC Evolutionary Biology.

[35]  Lewis G. Spurgin,et al.  MHC heterozygosity and survival in red junglefowl , 2010, Molecular ecology.

[36]  J. Merilä,et al.  Rhh: an R extension for estimating multilocus heterozygosity and heterozygosity–heterozygosity correlation , 2010, Molecular ecology resources.

[37]  M. Reichard,et al.  MATE CHOICE FOR NONADDITIVE GENETIC BENEFITS CORRELATE WITH MHC DISSIMILARITY IN THE ROSE BITTERLING (RHODEUS OCELLATUS) , 2010, Evolution; international journal of organic evolution.

[38]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[39]  M. Raymond,et al.  MHC, mate choice and heterozygote advantage in a wild social primate , 2010, Molecular ecology.

[40]  Jennifer J. Lhost,et al.  MHC Heterozygote Advantage in Simian Immunodeficiency Virus–Infected Mauritian Cynomolgus Macaques , 2010, Science Translational Medicine.

[41]  B. Neff,et al.  Major histocompatibility complex heterozygote advantage and widespread bacterial infections in populations of Chinook salmon (Oncorhynchus tshawytscha) , 2009, Molecular ecology.

[42]  Menna E. Jones,et al.  Life-history change in disease-ravaged Tasmanian devil populations , 2008, Proceedings of the National Academy of Sciences.

[43]  Katherine Belov,et al.  Transmission of a fatal clonal tumor by biting occurs due to depleted MHC diversity in a threatened carnivorous marsupial , 2007, Proceedings of the National Academy of Sciences.

[44]  H. Araki,et al.  Genetic Effects of Captive Breeding Cause a Rapid, Cumulative Fitness Decline in the Wild , 2007, Science.

[45]  E. Petersson,et al.  Influence of genetic dissimilarity in the reproductive success and mate choice of brown trout – females fishing for optimal MHC dissimilarity , 2007, Journal of evolutionary biology.

[46]  R. Sharpe,et al.  The Pathology of Devil Facial Tumor Disease (DFTD) in Tasmanian Devils (Sarcophilus harrisii) , 2006, Veterinary pathology.

[47]  J. Aparicio,et al.  What should we weigh to estimate heterozygosity, alleles or loci? , 2006, Molecular ecology.

[48]  L. Simmons,et al.  Sexual selection and mate choice. , 2006, Trends in ecology & evolution.

[49]  J. Höglund,et al.  Major histocompatibility complex variation and mate choice in a lekking bird, the great snipe (Gallinago media) , 2004, Molecular ecology.

[50]  E. Wapstra,et al.  Major histocompatibility complex and mate choice in sand lizards , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[51]  T. Glenn,et al.  Tetranucleotide microsatellite DNA loci from the dollar sunfish (Lepomis marginatus) , 2002 .

[52]  R. Daza,et al.  Genetics of the immune response: identifying immune variation within the MHC and throughout the genome , 2002, Immunological reviews.

[53]  C. Wedekind Sexual Selection and Life‐History Decisions: Implications for Supportive Breeding and the Management of Captive Populations , 2002 .

[54]  M. Milinski,et al.  Female sticklebacks count alleles in a strategy of sexual selection explaining MHC polymorphism , 2001, Nature.

[55]  P. Hedrick,et al.  Parasite resistance and genetic variation in the endangered Gila topminnow , 2001 .

[56]  M. Krawczak,et al.  Increased reproductive success of MHC class II heterozygous males among free-ranging rhesus macaques , 2001, Human Genetics.

[57]  E. Keverne,et al.  Genetic imprinting: Urinary odour preferences in mice , 2001, Nature.

[58]  J. Sambrook,et al.  Molecular Cloning: A Laboratory Manual , 2001 .

[59]  Markus Schuelke,et al.  An economic method for the fluorescent labeling of PCR fragments , 2000, Nature Biotechnology.

[60]  W. Potts,et al.  The Evolution of Mating Preferences and Major Histocompatibility Complex Genes , 1999, The American Naturalist.

[61]  J. Pemberton,et al.  No evidence for major histocompatibility complex–dependent mating patterns in a free–living ruminant population , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[62]  C. Wedekind,et al.  MHC-dependent mate preferences in humans , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[63]  J. Epplen,et al.  Typing of artiodactyl MHC‐DRB genes with the help of intronic simple repeated DNA sequences , 1993, Molecular ecology.

[64]  Jerram L. Brown,et al.  The major histocompatibility complex and female mating preferences in mice , 1989, Animal Behaviour.

[65]  B J Mathieson,et al.  Control of mating preferences in mice by genes in the major histocompatibility complex , 1976, The Journal of experimental medicine.

[66]  R. Zinkernagel,et al.  Enhanced immunological surveillance in mice heterozygous at the H-2 gene complex , 1975, Nature.

[67]  C. Hogg,et al.  Metapopulation management of an Endangered species with limited genetic diversity in the presence of disease: the Tasmanian devil Sarcophilus harrisii , 2017 .

[68]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[69]  C. Asa,et al.  Can conservation‐breeding programmes be improved by incorporating mate choice? , 2011 .

[70]  D. Kleiman,et al.  Wild mammals in captivity : principles and techniques for zoo management , 2010 .

[71]  K. Abbott,et al.  Opposites attract: MHC‐associated mate choice in a polygynous primate , 2010, Journal of evolutionary biology.

[72]  K. P. Murphy,et al.  Janeway's immunobiology , 2007 .

[73]  Jerram L. Brown A theory of mate choice based on heterozygosity , 1997 .

[74]  J. Klein Natural history of the major histocompatibility complex , 1986 .