Social and genetic interactions drive fitness variation in a free-living dolphin population

The evolutionary forces that drive fitness variation in species are of considerable interest. Despite this, the relative importance and interactions of genetic and social factors involved in the evolution of fitness traits in wild mammalian populations are largely unknown. To date, a few studies have demonstrated that fitness might be influenced by either social factors or genes in natural populations, but none have explored how the combined effect of social and genetic parameters might interact to influence fitness. Drawing from a long-term study of wild bottlenose dolphins in the eastern gulf of Shark Bay, Western Australia, we present a unique approach to understanding these interactions. Our study shows that female calving success depends on both genetic inheritance and social bonds. Moreover, we demonstrate that interactions between social and genetic factors also influence female fitness. Therefore, our study represents a major methodological advance, and provides critical insights into the interplay of genetic and social parameters of fitness.

[1]  M. Heithaus SHARK ATTACKS ON BOTTLENOSE DOLPHINS (TURSIOPS ADUNCUS) IN SHARK BAY, WESTERN AUSTRALIA: ATTACK RATE, BITE SCAR FREQUENCIES, AND ATTACK SEASONALITY , 2001 .

[2]  Elissa Z Cameron,et al.  Social bonds between unrelated females increase reproductive success in feral horses , 2009, Proceedings of the National Academy of Sciences.

[3]  R. Connor,et al.  Habituated Dolphins (Tursiops sp.) in Western Australia , 1985 .

[4]  W. G. Hill,et al.  Modification of Estimates of Parameters in the Construction of Genetic Selection Indices ('Bending') , 1981 .

[5]  J. Mann,et al.  Contrasting relatedness patterns in bottlenose dolphins (Tursiops sp.) with different alliance strategies , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[6]  M. Heithaus Predator–prey and competitive interactions between sharks (order Selachii) and dolphins (suborder Odontoceti): a review , 2001 .

[7]  S. Iverson,et al.  MATERNAL EFFECTS ON OFFSPRING MASS AND STAGE OF DEVELOPMENT AT BIRTH IN THE HARBOR SEAL, PHOCA VITULINA , 2000 .

[8]  A. Essl Choice of an appropriate bending factor using prior knowledge of the parameters , 1991 .

[9]  Steven J. Schwager,et al.  A comparison of association indices , 1987, Animal Behaviour.

[10]  M. Feldman,et al.  Gene-culture coevolutionary theory. , 1996, Trends in ecology & evolution.

[11]  D. Blumstein,et al.  Red kangaroos (Macropus rufus) receive an antipredator benefit from aggregation , 2003, acta ethologica.

[12]  J. Mann,et al.  Home range overlap, matrilineal and biparental kinship drive female associations in bottlenose dolphins , 2010, Animal Behaviour.

[13]  Céline Teplitsky,et al.  Heritability of Fitness Components in a Wild Bird Population , 2009, Evolution; international journal of organic evolution.

[14]  J. Mann,et al.  Developmental evidence for foraging traditions in wild bottlenose dolphins , 2009, Animal Behaviour.

[15]  A. J. Moore,et al.  Evolutionary consequences of indirect genetic effects. , 1998, Trends in ecology & evolution.

[16]  R. Harcourt,et al.  Shared Reproductive State Enhances Female Associations in Dolphins , 2008 .

[17]  Janet Mann Barbara BEHAVIORAL DEVELOPMENT IN WILD BOTTLENOSE DOLPHIN NEWBORNS (TURSIOPS SP.) , 1999 .

[18]  A. Harcourt The Chimpanzees of Gombe. Patterns of Behavior, Jane Goodall. Belknap Press of Harvard University Press, Cambridge, Massachussets (1986), xii, +671. Price $30 , 1988 .

[19]  B. L. Boeuf,et al.  Life history consequences of variation in age at primiparity in northern elephant seals , 1991, Behavioral Ecology and Sociobiology.

[20]  A. J. Moore,et al.  INTERACTING PHENOTYPES AND THE EVOLUTIONARY PROCESS: I. DIRECT AND INDIRECT GENETIC EFFECTS OF SOCIAL INTERACTIONS , 1997, Evolution; international journal of organic evolution.

[21]  J. Silk Social Components of Fitness in Primate Groups , 2007, Science.

[22]  Terry Burke,et al.  Pedigree-free animal models: the relatedness matrix reloaded , 2008, Proceedings of the Royal Society B: Biological Sciences.

[23]  Jeanne Altmann,et al.  Social Bonds of Female Baboons Enhance Infant Survival , 2003, Science.

[24]  K. Laland,et al.  How culture shaped the human genome: bringing genetics and the human sciences together , 2010, Nature Reviews Genetics.

[25]  Randall S. Wells,et al.  The Social Structure of Free-Ranging Bottlenose Dolphins , 1987 .

[26]  R. Fernando,et al.  Linear models for joint association and linkage QTL mapping , 2009, Genetics Selection Evolution.

[27]  D. Houle Comparing evolvability and variability of quantitative traits. , 1992, Genetics.

[28]  Mollie E. Brooks,et al.  Generalized linear mixed models: a practical guide for ecology and evolution. , 2009, Trends in ecology & evolution.

[29]  S. Ridgway,et al.  The second book of dolphins and the porpoises , 1999 .

[30]  L L Cavalli-Sforza,et al.  Paradox of the evolution of communication and of social interactivity. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Mark Kirkpatrick,et al.  Better Estimates of Genetic Covariance Matrices by “Bending” Using Penalized Maximum Likelihood , 2010, Genetics.

[32]  L. Kruuk,et al.  Heritability of fitness in a wild mammal population. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[33]  J. Mann,et al.  Cultural transmission of tool use in bottlenose dolphins. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[34]  C. Bradshaw,et al.  Harem choice and breeding experience of female southern elephant seals influence offspring survival , 2004, Behavioral Ecology and Sociobiology.

[35]  Jarrod D. Hadfield,et al.  The Misuse of BLUP in Ecology and Evolution , 2009, The American Naturalist.

[36]  M W Feldman,et al.  Toward a theory for the evolution of cultural communication: coevolution of signal transmission and reception. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[37]  W. Sherwin,et al.  Population structure in an inshore cetacean revealed by microsatellite and mtDNA analysis: Bottlenose dolphins (Tursiops sp.) in Shark Bay, Western Australia , 2004 .

[38]  Hal Whitehead,et al.  SOCPROG programs: analysing animal social structures , 2009, Behavioral Ecology and Sociobiology.

[39]  G. Blomquist Fitness-related patterns of genetic variation in rhesus macaques , 2009, Genetica.

[40]  J. Silk,et al.  The adaptive value of sociality in mammalian groups , 2007, Philosophical Transactions of the Royal Society B: Biological Sciences.

[41]  John W. Pepper,et al.  Sex Differences in Patterns of Association Among Indian Ocean Bottlenose Dolphins , 1992 .

[42]  D. Roff,et al.  Quantitative genetics and fitness: lessons from Drosophila , 1987, Heredity.

[43]  S. Allen,et al.  Association patterns and kinship in female Indo-Pacific bottlenose dolphins (Tursiops aduncus) of southeastern Australia , 2006, Behavioral Ecology and Sociobiology.

[44]  J. V. van Arendonk,et al.  Estimating Breeding Values With Molecular Relatedness and Reconstructed Pedigrees in Natural Mating Populations of Common Sole, Solea Solea , 2010, Genetics.

[45]  Kevin N Laland,et al.  Exploring gene–culture interactions: insights from handedness, sexual selection and niche-construction case studies , 2008, Philosophical Transactions of the Royal Society B: Biological Sciences.

[46]  G. McCracken,et al.  ON ESTIMATING RELATEDNESS USING GENETIC MARKERS , 1985, Evolution; international journal of organic evolution.

[47]  C. Schaik,et al.  The socioecology of fission-fusion sociality in Orangutans , 2007, Primates.

[48]  J. Mann,et al.  Female reproductive success in bottlenose dolphins (Tursiops sp.): life history, habitat, provisioning, and group-size effects , 2000 .

[49]  L. Kruuk Estimating genetic parameters in natural populations using the "animal model". , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.