Survival benefits select for group living in a social spider despite reproductive costs

The evolution of cooperation requires benefits of group living to exceed costs. Hence, some components of fitness are expected to increase with increasing group size, whereas others may decrease because of competition among group members. The social spiders provide an excellent system to investigate the costs and benefits of group living: they occur in groups of various sizes and individuals are relatively short‐lived, therefore life history traits and Lifetime Reproductive Success (LRS) can be estimated as a function of group size. Sociality in spiders has originated repeatedly in phylogenetically distant families and appears to be accompanied by a transition to a system of continuous intra‐colony mating and extreme inbreeding. The benefits of group living in such systems should therefore be substantial. We investigated the effect of group size on fitness components of reproduction and survival in the social spider Stegodyphus dumicola in two populations in Namibia. In both populations, the major benefit of group living was improved survival of colonies and late‐instar juveniles with increasing colony size. By contrast, female fecundity, female body size and early juvenile survival decreased with increasing group size. Mean individual fitness, estimated as LRS and calculated from five components of reproduction and survival, was maximized for intermediate‐ to large‐sized colonies. Group living in these spiders thus entails a net reproductive cost, presumably because of an increase in intra‐colony competition with group size. This cost is traded off against survival benefits at the colony level, which appear to be the major factor favouring group living. In the field, many colonies occur at smaller size than expected from the fitness curve, suggesting ecological or life history constraints on colony persistence which results in a transient population of relatively small colonies.

[1]  Robert M. May,et al.  Dispersal in stable habitats , 1977, Nature.

[2]  Thomas Caraco,et al.  Risk‐Sensitivity and Foraging Groups , 1981 .

[3]  E. Vargo,et al.  Inbreeding and disease resistance in a social insect: effects of heterozygosity on immunocompetence in the termite Zootermopsis angusticollis , 2006, Proceedings of the Royal Society B: Biological Sciences.

[4]  A. Griffin,et al.  Social evolution theory for microorganisms , 2006, Nature Reviews Microbiology.

[5]  Florian Jeltsch,et al.  Modelling individual variability in a social spider colony (Stegodyphus dumicola: Eresidae) in relation to food abundance and its allocation , 1996 .

[6]  W. Hamilton,et al.  The evolution of cooperation. , 1984, Science.

[7]  A. Griffin,et al.  Kin selection: fact and fiction , 2002 .

[8]  Karin Ulbrich,et al.  Intraspecific competition in a social spider , 1999 .

[9]  Stephen T. Emlen,et al.  Cooperative breeding in birds and mammals. , 1984 .

[10]  B. Crespi,et al.  The Evolution of Social Behavior in Insects and Arachnids: Explanation and evolution of social systems , 1997 .

[11]  J. Herbers Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus , 1986, Behavioral Ecology and Sociobiology.

[12]  M. Whitehouse,et al.  FOOD CONSUMPTION RATES AND COMPETITION IN A COMMUNALLY FEEDING SOCIAL SPIDER, STEGODYPHUS DUMICOLA (ERESIDAE) , 2000 .

[13]  Leticia Avilés,et al.  The Evolution of Social Behavior in Insects and Arachnids: Causes and consequences of cooperation and permanent-sociality in spiders , 1997 .

[14]  Ann L. Rypstra,et al.  Prey Size, Social Competition, and the Development of Reproductive Division of Labor in Social Spider Groups , 1993, The American Naturalist.

[15]  J. M. Smith,et al.  Group Selection , 1976, The Quarterly Review of Biology.

[16]  Leticia Avilés,et al.  Nomadic behaviour and colony fission in a cooperative spider: life history evolution at the level of the colony? , 2000 .

[17]  L. Keller Social evolution in ants , 1996 .

[18]  J. Heinze Habitat structure, dispersal strategies and queen number in two boreal Leptothorax ants , 1993, Oecologia.

[19]  Leticia Avilés,et al.  Interdemic Selection and the Sex Ratio: A Social Spider Perspective , 1993, The American Naturalist.

[20]  L. Avilés,et al.  Natal dispersal and demography of a subsocial Anelosimus species and its implications for the evolution of sociality in spiders , 1998 .

[21]  Y. Lubin,et al.  Cooperative breeding increases reproductive success in the social spider Stegodyphus dumicola (Araneae, Eresidae) , 2007, Behavioral Ecology and Sociobiology.

[22]  F. Vollrath Colony Foundation in a Social Spider , 1982 .

[23]  T. Bilde,et al.  THE TRANSITION TO SOCIAL INBRED MATING SYSTEMS IN SPIDERS: ROLE OF INBREEDING TOLERANCE IN A SUBSOCIAL PREDECESSOR , 2005, Evolution; international journal of organic evolution.

[24]  W. Wickler,et al.  Why do "family spiders", Stegodyphus (Eresidae), live in colonies? , 1988 .

[25]  R. Frankham,et al.  Most species are not driven to extinction before genetic factors impact them. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[26]  G. Gerlach,et al.  Reproductive skew, costs, and benefits of cooperative breeding in female wood mice (Apodemus sylvaticus) , 2002 .

[27]  Y. Lubin,et al.  Population stability and extinction in a social spider Stegodyphus mimosarum (Araneae: Eresidae) , 2001 .

[28]  P. Ward Prey Availability Increases Less Quickly Than Nest Size in the Social Spider Stegodyphus Mimosarum , 1986 .

[29]  P. Ward,et al.  Conflict and Cooperation in the Group Feeding of the Social Spider Stegodyphus Mimosarum , 1985 .

[30]  E. Leigh,et al.  2. Levels of Selection, Potential Conflicts, and Their Resolution: The Role of the “Common Good” , 2000 .

[31]  M. A. Noordwijk,et al.  The effects of dominance rank and group size on female lifetime reproductive success in wild long-tailed macaques,Macaca fascicularis , 2007, Primates.

[32]  T. Bilde,et al.  The Evolution of Sociality in Spiders , 2007 .

[33]  L. Keller,et al.  Inbreeding effects in wild populations. , 2002 .

[34]  T. Clutton‐Brock Cooperative breeding in mammals , 2006 .

[35]  Leticia Avilés,et al.  Sex-Ratio Bias and Possible Group Selection in the Social Spider Anelosimus eximius , 1986, The American Naturalist.

[36]  Yael Lubin,et al.  DISPERSAL OF STEGODYPHUS DUMICOLA (ARANEAE, ERESIDAE): THEY DO BALLOON AFTER ALL! , 2001 .

[37]  A. Griffin,et al.  Kin Discrimination and the Benefit of Helping in Cooperatively Breeding Vertebrates , 2003, Science.

[38]  J. Coddington,et al.  SOCIALITY IN THERIDIID SPIDERS: REPEATED ORIGINS OF AN EVOLUTIONARY DEAD END , 2006, Evolution; international journal of organic evolution.

[39]  L Avilés,et al.  Colony Size and Individual Fitness in the Social Spider Anelosimus eximius , 1998, The American Naturalist.

[40]  T. Caraco,et al.  Resource Consumption Variance Within and Among Individuals: On Coloniality in Spiders , 1995 .

[41]  M. Taborsky,et al.  Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid , 2004, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[42]  E. Kullmann Evolution of Social Behavior in Spiders (Araneae; Eresidae and Theridiidae) , 1972 .

[43]  A. Dhondt,et al.  Genetic diversity predicts pathogen resistance and cell-mediated immunocompetence in house finches , 2005, Biology Letters.

[44]  Y. Lubin,et al.  Sexual competition in an inbreeding social spider,Stegodyphus dumicola (Araneae: Eresidae) , 1995, Insectes Sociaux.

[45]  Samir Okasha,et al.  MULTILEVEL SELECTION AND THE PARTITIONING OF COVARIANCE: A COMPARISON OF THREE APPROACHES , 2004, Evolution; international journal of organic evolution.

[46]  Deborah Charlesworth,et al.  INBREEDING DEPRESSION AND ITS EVOLUTIONARY CONSEQUENCES , 1987 .

[47]  W. Wickler,et al.  Gerontophagy versus cannibalism in the social spiders Stegodyphus mimosarum Pavesi and Stegodyphus dumicola Pocock , 1987, Animal Behaviour.

[48]  Derek A Roff,et al.  Inbreeding depression in the wild , 1999, Heredity.

[49]  R. Tercafs Cooperative breeding in birds: Long-Term Studies of Ecology; Behavior: Peter B. Stacey; Walter D. Koenig. Cambridge University Press; UK. 1990. 615 pp. ISBN 0-521-37890-7 , 1991 .

[50]  R. R. Krausz Living in Groups , 2013 .

[51]  Robert M. May,et al.  Group selection , 1975, Nature.

[52]  L. Keller,et al.  Partitioning of reproduction in animal societies. , 1994, Trends in ecology & evolution.

[53]  J. Vasconcellos‐Neto,et al.  Female body size, fecundity parameters and foundation of new colonies in Anelosimus jabaquara (Araneae, Theridiidae) , 2001, Insectes Sociaux.

[54]  D. Charlesworth,et al.  Effects of a change in the level of inbreeding on the genetic load , 1991, Nature.

[55]  W. Koenig,et al.  Reproductive Success, Group Size, and the Evolution of Cooperative Breeding in the Acorn Woodpecker , 1981, The American Naturalist.

[56]  J. Henschel Is solitary life an alternative for the social spider stegodyphus dumicola , 1992 .

[57]  L. Avilés,et al.  Group living and inbreeding depression in a subsocial spider , 2006, Proceedings of the Royal Society B: Biological Sciences.

[58]  M. Wade Kin selection: its components. , 1980, Science.

[59]  B. Stutchbury,et al.  Choice of colony size in birds. , 1990, Trends in ecology & evolution.

[60]  E. Wilson,et al.  The number of queens: An important trait in ant evolution , 2004, Naturwissenschaften.

[61]  Eörs Szathmáry,et al.  The Major Transitions in Evolution , 1997 .

[62]  D. Smith,et al.  Population structure and interdemic selection in the cooperative spider Anelosimus eximius , 1996 .

[63]  J. Henschel PREDATION ON SOCIAL AND SOLITARY INDIVIDUALS OF THE SPIDER STEGODYPHUS DUMICOLA (ARANEAE, ERESIDAE) , 1998 .

[64]  S. Barrett,et al.  PERSPECTIVE: PURGING THE GENETIC LOAD: A REVIEW OF THE EXPERIMENTAL EVIDENCE , 2002, Evolution; international journal of organic evolution.

[65]  R. D. Alexander,et al.  The evolution of social behavior , 1974 .

[66]  C. Clark,et al.  The evolutionary advantages of group foraging , 1986 .

[67]  T. Bilde,et al.  The age and evolution of sociality in Stegodyphus spiders: a molecular phylogenetic perspective , 2007, Proceedings of the Royal Society B: Biological Sciences.

[68]  Laurent Keller,et al.  Levels of Selection: Burying the Units-of-Selection Debate and Unearthing the Crucial New Issues , 2000 .

[69]  A. Bourke,et al.  The Ecology of Communal Breeding: The Case of Multiple-Queen Leptothoracine Ants , 1994 .

[70]  The origin of helping: the role of variability in reproductive potential. , 1985, Journal of theoretical biology.

[71]  P. Sherman,et al.  DNA "fingerprinting" reveals high levels of inbreeding in colonies of the eusocial naked mole-rat. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[72]  Y. Lubin,et al.  Trial by fire: social spider colony demographics in periodically burned grassland , 2003 .

[73]  Y. Lubin,et al.  Competitive foraging in the social spider Stegodyphus dumicola , 1999, Animal Behaviour.

[74]  R. Frankham,et al.  Does Inbreeding and Loss of Genetic Diversity Decrease Disease Resistance? , 2004, Conservation Genetics.

[75]  W. Wickler,et al.  Bionomics and social structure of 'Family Spiders' of the genus Stegodyphus, with special reference to the African species S.dumicola and S.mimosarum (Araneida, Eresidae) , 1988 .

[76]  D. Queller,et al.  Does population viscosity promote kin selection? , 1992, Trends in ecology & evolution.

[77]  D. Hasselquist,et al.  Inbreeding effects on immune response in free-living song sparrows (Melospiza melodia) , 2006, Proceedings of the Royal Society B: Biological Sciences.

[78]  J. Johannesen,et al.  Mitochondrial DNA distributions indicate colony propagation by single matri‐lineages in the social spider Stegodyphus dumicola (Eresidae) , 2002 .

[79]  R. Buskirk 4 – Sociality in the Arachnida , 1981 .

[80]  J. Bundgaard,et al.  Environmental dependence of inbreeding depression and purging in Drosophila melanogaster , 1999 .

[81]  Lars Gustafsson,et al.  Single‐Generation Estimates of Individual Fitness as Proxies for Long‐Term Genetic Contribution , 2004, The American Naturalist.

[82]  George Williams Group Selection , 1971 .

[83]  Leticia Avilés,et al.  Cooperation and non-linear dynamics: An ecological perspective on the evolution of sociality , 1999 .