Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution

Eusociality is taxonomically rare, yet associated with great ecological success. Surprisingly, studies of environmental conditions favouring eusociality are often contradictory. Harsh conditions associated with increasing altitude and latitude seem to favour increased sociality in bumblebees and ants, but the reverse pattern is found in halictid bees and polistine wasps. Here, we compare the life histories and distributions of populations of 176 species of Hymenoptera from the Swiss Alps. We show that differences in altitudinal distributions and development times among social forms can explain these contrasting patterns: highly social taxa develop more quickly than intermediate social taxa, and are thus able to complete the reproductive cycle in shorter seasons at higher elevations. This dual impact of altitude and development time on sociality illustrates that ecological constraints can elicit dynamic shifts in behaviour, and helps explain the complex distribution of sociality across ecological gradients.

[1]  A. Cronin,et al.  Social polymorphism in the sweat bee Lasioglossum (Evylaeus) baleicum (Cockerell) (Hymenoptera, Halictidae) in Hokkaido, northern Japan , 2003, Insectes Sociaux.

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

[3]  L. Packer,et al.  Population-typical behaviours are retained when eusocial and non-eusocial forms of Evylaeus albipes (F.) (Hymenoptera, Halictidae) are reared simultaneously in the laboratory , 2000, Insectes Sociaux.

[4]  J. Bosch,et al.  Development and Emergence of the Alfalfa Pollinator Megachile rotundata (Hymenoptera: Megachilidae) , 2000 .

[5]  R. B. Roberts Biology of the Bee Genus Agapostemon (Hymenoptera: Halictidae) , 1969 .

[6]  Raphaël Jeanson,et al.  Emergence of increased division of labor as a function of group size , 2007, Behavioral Ecology and Sociobiology.

[7]  M. Schwarz,et al.  The habitat saturation hypothesis and sociality in an allodapine bee: cooperative nesting is not “making the best of a bad situation” , 1996, Behavioral Ecology and Sociobiology.

[8]  Patricio A. Salazar,et al.  Altitudinal Patterns of Spider Sociality and the Biology of a New Midelevation Social Anelosimus Species in Ecuador , 2007, The American Naturalist.

[9]  D. Janzen Why Mountain Passes are Higher in the Tropics , 1967, The American Naturalist.

[10]  S. Higashi,et al.  Degree-day accumulation controlling allopatric and sympatric variations in the sociality of sweat bees, Lasioglossum (Evylaeus) baleicum (Hymenoptera: Halictidae) , 2008, Behavioral Ecology and Sociobiology.

[11]  L. Packer Solitary and eusocial nests in a population of Augochlorella striata (Provancher) (Hymenoptera; Halictidae) at the northern edge of its range , 1990, Behavioral Ecology and Sociobiology.

[12]  A. Dornhaus,et al.  Ambient Air Temperature Does Not Predict whether Small or Large Workers Forage in Bumble Bees (Bombus impatiens) , 2010, Psyche; a journal of entomology.

[13]  B. Danforth,et al.  PHYLOGEOGRAPHY OF THE SOCIALLY POLYMORPHIC SWEAT BEE HALICTUS RUBICUNDUS (HYMENOPTERA: HALICTIDAE) , 2002, Evolution; international journal of organic evolution.

[14]  A. Bourke Sex ratios in bumble bees , 1997 .

[15]  Victor H. Gonzalez,et al.  The evolution of nocturnal behaviour in sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera: Halictidae): an escape from competitors and enemies? , 2004 .

[16]  M. Richards Nesting biology and social organization of Halictus sexcinctus (Fabricius) in southern Greece , 2001 .

[17]  Charles D. Michener,et al.  The Social Behavior of the Bees , 1974 .

[18]  S. Sakagami,et al.  Distribution and Bionomics of a Transpalaearctic Eusocial Halictine Bee, Lasioglossum (Evylaeus) calceatum, in Northern Japan, with Reference to Its Solitary Life Cycle at High Altitude (With 9 Text-figures and 2 Tables) , 1972 .

[19]  W. Wcislo,et al.  Social and ecological contexts of trophallaxis in facultatively social sweat bees, Megalopta genalis and M. ecuadoria (Hymenoptera, Halictidae) , 2006, Insectes Sociaux.

[20]  R. Cumber THE BIOLOGY OF HUMBLE-BEES, WITH SPECIAL REFERENCE TO THE PRODUCTION OF THE WORKER CASTE. , 2009 .

[21]  S. Turillazzi,et al.  Behavioural and ecological adaptations to the high mountain environment of Polistes biglumis bimaculatus , 1986 .

[22]  H. Poethke,et al.  Risk-sensitive foraging and the evolution of cooperative breeding and reproductive skew , 2008, BMC Ecology.

[23]  M. Schwarz,et al.  Social complexity in bees is not sufficient to explain lack of reversions to solitary living over long time scales , 2007, BMC Evolutionary Biology.

[24]  S. Sakagami,et al.  Geographical variation of sociality and size-linked color patterns in Lasioglossum (Evylaeus) apristum (Vachal) in Japan (Hymenoptera, Halictidae) , 1999, Insectes Sociaux.

[25]  C. H. Dodson Ethology of Some Bees of the Tribe Euglossini (Hymenoptera: Apidae) , 1966 .

[26]  Joel P. Brockman,et al.  What is Bet-Hedging , 1987 .

[27]  D. Fairbairn,et al.  Macroevolutionary patterns of bumblebee body size: detecting the interplay between natural and sexual selection , 2012, Ecology and evolution.

[28]  W. Wcislo,et al.  Nesting biology of tropical solitary and social sweat bees,Lasioglossum (Dialictus) figueresi Wcislo andL. (D.) aeneiventre (Friese) (Hymenoptera: Halictidae) , 1993, Insectes Sociaux.

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

[30]  R. D. McMullen,et al.  FACTORS AFFECTING INDUCTION AND TERMINATION OF DIAPAUSE IN PEAR PSYLLA (HOMOPTERA: PSYLLIDAE) , 1976, The Canadian Entomologist.

[31]  C. Michener,et al.  Nests and Social Behavior of Three Species of Pseudaugochloropsis (Hymenoptera: Halictidae) , 1967 .

[32]  M. Breed THE EVOLUTION OF SOCIAL BEHAVIOR IN PRIMITIVELY SOCIAL BEES: A MULTIVARIATE ANALYSIS , 1976, Evolution; international journal of organic evolution.

[33]  R. Moritz,et al.  Workers dominate male production in the neotropical bumblebee Bombus wilmattae (Hymenoptera: Apidae) , 2011, Frontiers in Zoology.

[34]  L. Packer Multiple-foundress associations in a temperate population of Halictus ligatus (Hymenoptera; Halictidae) , 1986 .

[35]  C. A. Garófalo,et al.  Nesting behaviour of Centris (Heterocentris) analis (Fabricius) in southeastern Brazil (Hymenoptera, Apidae, Centridini) , 2000 .

[36]  R. Moritz,et al.  Mating frequency and genetic colony structure of the neotropical bumblebee Bombus wilmattae (Hymenoptera: Apidae) , 2011, Apidologie.

[37]  Michael Kaspari,et al.  Colony Size as a Buffer Against Seasonality: Bergmann's Rule in Social Insects , 1994, The American Naturalist.

[38]  W. Wcislo,et al.  Solitary behavior in a high-altitude population of the social sweat bee Halictus rubicundus (Hymenoptera: Halictidae) , 1996, Behavioral Ecology and Sociobiology.

[39]  N. Zimmermann,et al.  Predictive mapping of alpine grasslands in Switzerland: Species versus community approach , 1999 .

[40]  D. Yanega,et al.  Social plasticity and early-diapausing females in a primitively social bee. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[41]  L. Packer,et al.  The Evolution of Social Behavior in Insects and Arachnids , 1998 .

[42]  C. Polidori,et al.  Biology of Lasioglossum (L.) majus (Hymenoptera: Halictidae), a largely solitary sweat bee with behavioural adaptations to communality , 2009, Journal of Ethology.

[43]  F. D. Bennett Observations on Exaerete spp. and Their Hosts Eulaema terminata and Euplusia surinamensis (Hymen., Apidae, Euglossinae) in Trinidad , 1972 .

[44]  S. Dorn,et al.  Ecological and seasonal patterns in the diversity of a species-rich bee assemblage (Hymenoptera: Apoidea: Apiformes) , 2005 .

[45]  S. Sakagami Specific Differences in the Bionomic Characters of Bumblebees.:A Comparative Review (With 4 Text-figures) , 1976 .

[46]  T. Wenseleers,et al.  Comparative Analysis of Worker Reproduction and Policing in Eusocial Hymenoptera Supports Relatedness Theory , 2006, The American Naturalist.

[47]  M. Lindauer Ethology. , 1962, Annual review of psychology.

[48]  J. H. Hunt,et al.  A conceptual model for the origin of worker behaviour and adaptation of eusociality , 2012, Journal of evolutionary biology.

[49]  B. Inouye,et al.  Nesting Biology, Seasonality, and Mating Behavior of Epicharis metatarsalis (Hymenoptera: Apidae) in Northeastern Costa Rica , 2007 .

[50]  B. Danforth,et al.  The bee tree of life: a supermatrix approach to apoid phylogeny and biogeography , 2013, BMC Evolutionary Biology.

[51]  Dustin R. Rubenstein,et al.  Spatiotemporal environmental variation, risk aversion, and the evolution of cooperative breeding as a bet-hedging strategy , 2011, Proceedings of the National Academy of Sciences.

[52]  Paul R. Martin,et al.  Are mountain passes higher in the tropics? Janzen's hypothesis revisited. , 2006, Integrative and comparative biology.

[53]  H. Yoon,et al.  Temperature and humidity favorable for colony development of the indoor-reared bumblebee, Bombus ignitus , 2002 .

[54]  T. Laverty,et al.  COMPARATIVE BIONOMICS OF TEMPERATE AND TROPICAL BUMBLE BEES WITH SPECIAL REFERENCE TO BOMBUS EPHIPPIATUS (HYMENOPTERA: APIDAE) , 1985, The Canadian Entomologist.

[55]  J. Purcell,et al.  Smaller colonies and more solitary living mark higher elevation populations of a social spider. , 2007, The Journal of animal ecology.

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

[57]  R. Gadagkar Evolution of eusociality: the advantage of assured fitness returns , 1990 .

[58]  M. Schwarz,et al.  Evidence of Social Nesting in the Ceratina of Borneo (Hymenoptera: Apidae) , 2009 .

[59]  C. Rasmussen,et al.  Ecology and Nesting Behavior of Bombus atratus Franklin in Andean Highlands (Hymenoptera: Apidae) , 2004 .

[60]  G. Uetz Risk Sensitivity and the Paradox of Colonial Web-Building in Spiders , 1996 .

[61]  J. Schmidt,et al.  Colony development, larval development and worker reproduction in Bombus impatiens Cresson , 2002, Insectes Sociaux.

[62]  U. Mueller Life history and social evolution of the primitively eusocial bee Augochlorella striata (Hymenoptera: Halictidae) , 1996 .

[63]  G. Frankie,et al.  Nest Selection, Usurpation, and a Function for the Nest Entrance Plug of Centris bicornuta (Hymenoptera: Apidae) , 2000 .

[64]  R. Dudley,et al.  Into thin air: Physiology and evolution of alpine insects. , 2006, Integrative and comparative biology.

[65]  L. Packer,et al.  Social evolution and its correlates in bees of the subgenus Evylaeus (Hymenoptera; Halictidae) , 1985, Behavioral Ecology and Sociobiology.

[66]  J. Field,et al.  Cryptic Plasticity Underlies a Major Evolutionary Transition , 2010, Current Biology.

[67]  C. Plateaux-Qu Comparative biological data in two closely related eusocial species: Evylaeus calceatus (Scop.) and Evylaeus albipes (F.) (Hym., Halictinae) , 1992 .

[68]  P. Parker,et al.  Fostering model explains variation in levels of sociality in a spider system , 2007, Animal Behaviour.

[69]  D. Queller Extended parental care and the origin of eusociality , 1994, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[70]  M. Richards,et al.  Colony social organization of Lasioglossum malachurum Kirby (Hymenoptera, Halictidae) in southern Greece , 2003, Insectes Sociaux.

[71]  John B. Free,et al.  Bumblebee economics , 1979, Nature.

[72]  Sean O'Donnell,et al.  Thresholds of Response in Nest Thermoregulation by Worker Bumble Bees, Bombus bifarius nearcticus (Hymenoptera: Apidae) , 2001 .

[73]  D. Yanega The Evolution of Social Behavior in Insects and Arachnids: Demography and sociality in halictine bees (Hymenoptera: Halictidae) , 1997 .

[74]  R. Martins,et al.  Variability in egg‐to‐adult development time in the bee Ptilothrix plumata and its parasitoids , 2001 .

[75]  S. Potts,et al.  Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities , 2012, Proceedings of the Royal Society B: Biological Sciences.

[76]  S. Fucini,et al.  Social wasps without workers: geographic variation of caste expression in the paper wasp Polistes biglumis , 2009, Insectes Sociaux.

[77]  G. Amdam,et al.  Bivoltinism as an Antecedent to Eusociality in the Paper Wasp Genus Polistes , 2005, Science.

[78]  J. Purcell Geographic patterns in the distribution of social systems in terrestrial arthropods , 2011, Biological reviews of the Cambridge Philosophical Society.

[79]  J. Bosch,et al.  Development and Emergence of the Orchard Pollinator Osmia lignaria (Hymenoptera: Megachilidae) , 2000 .

[80]  C. Parmesan Ecological and Evolutionary Responses to Recent Climate Change , 2006 .