Colony nutrition skews reproduction in a social spider

Cooperative breeding societies are characterized by alloparental care and unequal distribution of reproduction (skewed reproduction). Competition for resources among group members may determine the reproductive outcome of each individual. In a spider colony, females feed together on prey and therefore may compete over the extraction of specific nutrients required for reproduction. Here we examined the occurrence of skewed reproduction in colonies of the social spider Stegodyphus dumicola (Eresidae) in nature and asked whether competition over specific limiting nutrients is a mechanism leading to unequal distribution of reproduction. We determined the nutritional composition of breeding and nonbreeding females in natural colonies. By supplementing field colonies with prey rich in either proteins or lipids, we examined the effect of these nutrients on female breeding potential. We then determined which nutrients were extracted from prey by breeding and nonbreeding females in a noncompetitive setting. About 40% of the females in natural colonies are potential breeders. Field colonies supplemented with lipid-rich prey had a higher percentage of breeding females than colonies supplemented with protein-rich prey. Furthermore, when feeding alone, nonbreeding females extracted more lipids relative to protein than breeding females. We suggest that lipids are critical for maturation and ovarian development and that competition for lipids determines the skewed reproduction observed in colonies of S. dumicola. Copyright 2008, Oxford University Press.

[1]  J. Ginsberg,et al.  Dominance, reproduction and survival in banded mongooses: towards an egalitarian social system? , 2001, Animal Behaviour.

[2]  Jerram L. Brown.  Alternate Routes to Sociality in Jays—With a Theory for the Evolution of Altruism and Communal Breeding , 1974 .

[3]  E. Dierenfeld,et al.  Nutrient composition of selected whole invertebrates , 1998 .

[4]  L. Avilés,et al.  Does the African social spider Stegodyphus dumicola control the sex of individual offspring? , 1999, Behavioral Ecology and Sociobiology.

[5]  D. Raubenheimer.  Problems with ratio analysis in nutritional studies , 1995 .

[6]  Stephen T. Emlen,et al.  The Evolution of Helping. I. An Ecological Constraints Model , 1982, The American Naturalist.

[7]  J. Schneider.  Survival and growth in groups of a subsocial spider (Stegodyphus lineatus) , 1995, Insectes Sociaux.

[8]  J. Strassmann,et al.  Physical variability among nest foundresses in the polygynous social wasp, Polistes annularis , 1984, Behavioral Ecology and Sociobiology.

[9]  Sandra L. Vehrencamp,et al.  A model for the evolution of despotic versus egalitarian societies , 1983, Animal Behaviour.

[10]  David Raubenheimer,et al.  Analysis of covariance: an alternative to nutritional indices , 1992 .

[11]  S. Vehrencamp.  Optimal Degree of Skew in Cooperative Societies , 1983 .

[12]  M. Keeping,et al.  Reproductive and worker castes in the primitively eusocial wasp Belonogaster petiolata (DeGeer) (Hymenoptera: Vespidae): evidence for pre-imaginal differentiation. , 2002, Journal of insect physiology.

[13]  A Griffin,et al.  Cooperation, control, and concession in meerkat groups. , 2001, Science.

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

[15]  Bernard J. Crespi,et al.  The Evolution of Social Behavior in Insects and Arachnids: Acknowledgements , 1997 .

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

[17]  H. Pulliam.  NATURAL SELECTION AND SOCIAL BEHAVIOR , 1982 .

[18]  T. Miyashita.  Variability in food consumption rate of natural populations in the spider,Nephila clavata , 1992, Researches on population ecology.

[19]  D. Wise.  Effects of an experimental increase in prey abundance upon the reproductive rates of two orb-weaving spider species (Araneae: Araneidae) , 1979, Oecologia.

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

[21]  John F Anderson.  Responses to Starvation in the Spiders Lycosa Lenta Hentz and Filistata Hibernalis (Hentz) , 1974 .

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

[23]  T. Bilde,et al.  Survival benefits select for group living in a social spider despite reproductive costs , 2007, Journal of evolutionary biology.

[24]  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 .

[25]  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.

[26]  D. Wheeler,et al.  The role of nourishment in oogenesis. , 1996, Annual review of entomology.

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

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

[29]  D. Wise.  Cannibalism, food limitation, intraspecific competition, and the regulation of spider populations. , 2006, Annual review of entomology.

[30]  R. Shuel,et al.  The early establishment of dimorphism in the female honeybee,Apis mellifera L. , 1960, Insectes Sociaux.

[31]  R. Chapman.  The Insects: Structure and Function , 1969 .

[32]  D. Macdonald.  The ecology of social behaviour , 1989 .

[33]  D. Wise.  Spiders in Ecological Webs , 1993 .

[34]  David Raubenheimer,et al.  Nutrient-Specific Foraging in Invertebrate Predators , 2005, Science.

[35]  M. Winston,et al.  THE ROLE OF NUTRITION AND TEMPERATURE IN THE OVARIAN DEVELOPMENT OF THE WORKER HONEY BEE (APIS MELLIFERA) , 1998, The Canadian Entomologist.

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

[37]  K. Collatz.  Structure and Function of the Digestive Tract , 1987 .

[38]  W. Wickler,et al.  Pedogenetic sociogenesis via the 'sibling-route' and some consequences for Stegodyphus spiders , 2010 .

[39]  M. West-Eberhard.  Flexible strategy and social evolution , 1987 .

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

[41]  F. Vollrath.  Eusociality and extraordinary sex ratios in the spider Anelosimus eximius (Araneae: Theridiidae) , 1986, Behavioral Ecology and Sociobiology.

[42]  Jerram L. Brown,et al.  Animal Societies: Theories and Facts , 1987 .

[43]  Kent H. Redford,et al.  The nutritional value of invertebrates with emphasis on ants and termites as food for mammals , 2009 .

[44]  W. Nentwig.  Ecophysiology of Spiders , 1987, Springer Berlin Heidelberg.

[45]  J. H. Hunt,et al.  Nourishment And Evolution In Insect Societies , 1994 .

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

[47]  J. Harwood,et al.  Web‐location by linyphiid spiders: prey‐specific aggregation and foraging strategies , 2003 .

[48]  H. Jane Brockmann,et al.  The Evolution of Social Behavior in Insects and Arachnids: Cooperative breeding in wasps and vertebrates: the role of ecological constraints , 1997 .

[49]  G. Uetz.  Chapter 15 – RISK SENSITIVITY AND FORAGING IN COLONIAL SPIDERS , 1988 .

[50]  J. Pennington,et al.  Fat metabolism in insects. , 2003, Annual review of nutrition.

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

[52]  J. Schneider,et al.  Reproductive state and care giving in Stegodyphus (Araneae: Eresidae) and the implications for the evolution of sociality , 2002, Animal Behaviour.

[53]  Allen Carson Cohen,et al.  Extra-Oral Digestion in Predaceous Terrestrial Arthropoda , 1995 .

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