Reproductive biology and genealogy in the endangered Iberian lynx: Implications for conservation

For endangered species, the availability of genealogies and a good knowledge of mating patterns are valuable resources for conservation purposes. Here we studied mating patterns in the endangered Iberian lynx, Lynx pardinus, and reconstructed a partial genealogy of the intensively monitored population in Donana from 1990 to 2013. Using microsatellites in combination with field information we assigned 146 out of the 175 analysed individuals to at least one parent with confidence above 0.9. We detected breeding events for 30% of individuals in the population (n = 181), which follows a positively skewed distribution (maximum: 7 breeding events for females, 9 for males). On average, individuals reproduce with approximately 1.6 mates in their life, from 2 years-old to a maximum of 10 years for males and 11 years for females. This broadening of the previously reported breeding age is likely due to stochastic changes in the demography that resulted in lack of competition and a high turnover of the territories. We identified several crosses between close relatives (e.g. full-sibs) which resulted in highly inbred offspring. To our knowledge, this is one of the most comprehensive studies on reproductive patterns of an endangered felid in the wild. This novel information highlights the importance of both field and genetic data to broaden the knowledge of the species and to improve conservation programs.

[1]  T. Clutton‐Brock,et al.  Male reproductive success in a promiscuous mammal: behavioural estimates compared with genetic paternity , 1999, Molecular ecology.

[2]  R. Wayne,et al.  The genealogy and genetic viability of reintroduced Yellowstone grey wolves , 2008, Molecular ecology.

[3]  J. Godoy,et al.  Heterozygosity‐Fitness Correlations and Inbreeding Depression in Two Critically Endangered Mammals , 2012, Conservation biology : the journal of the Society for Conservation Biology.

[4]  F. Palomares,et al.  Territoriality ensures paternity in a solitary carnivore mammal , 2017, Scientific Reports.

[5]  G. Garrote,et al.  Estimation of the Iberian lynx (Lynx pardinus) population in the Doñana area, SW Spain, using capture–recapture analysis of camera-trapping data , 2011, European Journal of Wildlife Research.

[6]  R. Sikes,et al.  Guidelines of the American Society of Mammalogists for the Use of Wild Mammals in Research , 2007 .

[7]  M. Hindell,et al.  Paternity analysis shows experience, not age, enhances mating success in an aquatically mating pinniped, the Weddell seal (Leptonychotes weddellii) , 2007, Behavioral Ecology and Sociobiology.

[8]  F. Palomares,et al.  Non cat-like ovarian cycle in the Eurasian and the Iberian lynx - ultrasonographical and endocrinological analysis. , 2009, Reproduction in domestic animals = Zuchthygiene.

[9]  O. Liberg,et al.  Severe inbreeding depression in a wild wolf Canis lupus population , 2005, Biology Letters.

[10]  J. DeWoody,et al.  Insights into the mating habits of the tiger salamander (Ambystoma tigrinum tigrinum) as revealed by genetic parentage analyses , 2006, Molecular ecology.

[11]  O. Liberg,et al.  Genetic rescue in a severely inbred wolf population , 2016, Molecular ecology.

[12]  P. Ferreras,et al.  Age determination of Iberian lynx (Lynx pardinus) using canine radiograph and cementum annuli enumeration , 1997 .

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

[14]  F. Palomares,et al.  Revisiting food-based models of territoriality in solitary predators. , 2014, The Journal of animal ecology.

[15]  R. Frankham,et al.  Genetic management of chondrodystrophy in California condors , 2000 .

[16]  P. Ferreras,et al.  Spatial organization and land tenure system of the endangered Iberian lynx (Lynx pardinus) , 1997 .

[17]  F. Balloux,et al.  Life history correlates of inbreeding depression in mandrills (Mandrillus sphinx) , 2005, Molecular ecology.

[18]  F. Palomares,et al.  Competitive Asymmetries in the Use of Supplementary Food by the Endangered Iberian Lynx (Lynx pardinus) , 2009, PloS one.

[19]  Jinlian Wang,et al.  COLONY: a program for parentage and sibship inference from multilocus genotype data , 2010, Molecular ecology resources.

[20]  Guillermo López,et al.  Feline Leukemia Virus and Other Pathogens as Important Threats to the Survival of the Critically Endangered Iberian Lynx (Lynx pardinus) , 2009, PloS one.

[21]  J. Pemberton,et al.  Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches , 2014, Molecular ecology.

[22]  F. Palomares,et al.  Intraspecific interference influences the use of prey hotspots , 2011 .

[23]  G. Garrote,et al.  First breeding record of a one-year-old female Iberian lynx , 2017, European Journal of Wildlife Research.

[24]  L. Bernatchez,et al.  Mating patterns and determinants of individual reproductive success in brown trout (Salmo trutta) revealed by parentage analysis of an entire stream living population , 2010, Molecular ecology.

[25]  Erlend B. Nilsen,et al.  The cost of maturing early in a solitary carnivore , 2010, Oecologia.

[26]  Alejandro Rodríguez,et al.  Field observation of two males following a female in the Iberian lynx (Lynx pardinus) during the mating season , 2008 .

[27]  W. Hödl,et al.  Strong male/male competition allows for nonchoosy females: high levels of polygynandry in a territorial frog with paternal care , 2011, Molecular ecology.

[28]  P. Gaona,et al.  DYNAMICS AND VIABILITY OF A METAPOPULATION OF THE ENDANGERED IBERIAN LYNX (LYNX PARDINUS) , 1998 .

[29]  E. Ågren,et al.  Reproductive maturation in the male Eurasian lynx (Lynx lynx): a study on 55 reproductive organs collected from carcasses during 2002-2005. , 2009, Reproduction in domestic animals = Zuchthygiene.

[30]  E. Roldán,et al.  Estudio de las poblaciones de carnívoros del Parque Nacional de Doñana usando métodos no invasivos , 2011 .

[31]  S. Durant,et al.  Genetic analysis reveals promiscuity among female cheetahs , 2007, Proceedings of the Royal Society B: Biological Sciences.

[32]  Francisco Palomares,et al.  Vegetation structure and prey abundance requirements of the Iberian lynx: implications for the design of reserves and corridors , 2001 .

[33]  E. Revilla,et al.  Possible Extinction Vortex for a Population of Iberian Lynx on the Verge of Extirpation , 2012, Conservation biology : the journal of the Society for Conservation Biology.

[34]  C. W. Kilpatrick,et al.  Kinship and social structure of bobcats (Lynx rufus) inferred from microsatellite and radio-telemetry data , 2006 .

[35]  E. Revilla,et al.  Reproduction and pre-dispersal survival of Iberian lynx in a subpopulation of the Doñana National Park , 2005 .

[36]  G. Jones,et al.  Relative accuracy of three common methods of parentage analysis in natural populations , 2013, Molecular ecology.

[37]  F. Palomares,et al.  Behavioural response of a trophic specialist, the Iberian lynx, to supplementary food: Patterns of food use and implications for conservation , 2008 .

[38]  R. Pong-Wong,et al.  Efficiency of the Use of Pedigree and Molecular Marker Information in Conservation Programs , 2005, Genetics.

[39]  J. Godoy,et al.  Genetics at the verge of extinction: insights from the Iberian lynx , 2013, Molecular ecology.

[40]  Dany Garant,et al.  How to use molecular marker data to measure evolutionary parameters in wild populations , 2005, Molecular ecology.

[41]  F. Palomares,et al.  Iberian lynx: the uncertain future of a critically endangered cat , 2010 .

[42]  E. Revilla,et al.  Assessment of the Conservation Efforts to Prevent Extinction of the Iberian Lynx , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[43]  S. H. Fritts,et al.  Reproductive biology and population characteristics of bobcats (Lynx rufus) in Arkansas. , 1978, Journal of mammalogy.

[44]  F. Palomares,et al.  Feline leukemia virus infection: A threat for the survival of the critically endangered Iberian lynx (Lynx pardinus) , 2009, Veterinary Immunology and Immunopathology.

[45]  Thorsten Wiegand,et al.  Individual movement behavior, matrix heterogeneity, and the dynamics of spatially structured populations , 2008, Proceedings of the National Academy of Sciences.

[46]  E. Revilla,et al.  Proximate and ultimate causes of dispersal in the Iberian lynx Lynx pardinus , 2004 .

[47]  J. Mann,et al.  The relative importance of reproduction and survival for the conservation of two dolphin populations , 2016, Ecology and evolution.

[48]  J. Godoy,et al.  A simple and effective method for obtaining mammal DNA from faeces , 2015 .

[49]  F. Palomares,et al.  Effects of food supplementation on home‐range size, reproductive success, productivity and recruitment in a small population of Iberian lynx , 2010 .

[50]  J. Pemberton,et al.  Wild pedigrees: the way forward , 2008, Proceedings of the Royal Society B: Biological Sciences.

[51]  F. Palomares,et al.  Feline leukaemia virus outbreak in the endangered Iberian lynx and the role of feeding stations: a cautionary tale , 2011 .

[52]  G. Garrote,et al.  Reverse of the Decline of the Endangered Iberian Lynx , 2012, Conservation biology : the journal of the Society for Conservation Biology.