Temperature drives caste-specific morphological clines in ants.
Bergmann's rule
Formicidae
climate
environmental gradients
functional traits
morphospace
Journal
The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
04
10
2019
accepted:
31
07
2020
pubmed:
29
8
2020
medline:
14
4
2021
entrez:
29
8
2020
Statut:
ppublish
Résumé
The morphology of organisms relates to most aspects of their life history and autecology. As such, elucidating the drivers of morphological variation along environmental gradients might give insight into processes limiting species distributions. In eusocial organisms, the concept of morphology is more complex than in solitary organisms. Eusocial insects such as ants exhibit drastic morphological differences between reproductive and worker castes. How environmental selection operates on the morphology of each caste, and whether caste-specific selection has fitness consequences is largely unknown, but is potentially crucial to understand what limits ant species' distributions. Here we aimed to examine whether ant shape and body size covaries with climate at the scale of an entire continent, and whether such relationship might be caste specific. We used 26,472 georeferenced morphometric measurements from 2,206 individual ants belonging to 32 closely related North American species in the genus Formica to assess how ant morphology relates to geographic variation in the abiotic environment. Although precipitation and seasonality explained some of the geographic variation in morphology, temperature was the best predictor. Specifically, geographic variation in body size was positively related to temperature, meaning that ants are smaller in cold than in warm environments. Moreover, the strength of the relationship between size and temperature was stronger for the reproductive castes (i.e. queens and males) than for the worker caste. The shape of workers and males also varied along these large-scale abiotic gradients. Specifically, the relative length of workers' legs, thoraxes and antennae positively related to temperature, meaning that they had shorter appendages in cold environments. In contrast, males had smaller heads, but larger thoraxes in more seasonal environments. Overall, our results suggest that geographic variation in ambient temperature influences the morphology of ants, but that the strength of this effect is caste specific. In conclusion, whereas ant ecology has traditionally focused on workers, our study shows that considering the ecology of the reproductive castes is imperative to move forward in this field.
Identifiants
pubmed: 32858759
doi: 10.1111/1365-2656.13330
doi:
Banques de données
Dryad
['10.5061/dryad.dncjsxkx3']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2517-2530Informations de copyright
© 2020 British Ecological Society.
Références
Abell, A. J., Cole, B. J., Reyes, R., & Wiernasz, D. C. (1999). Sexual selection on body size and shape in the western harvester ant, Pogonomyrmex occidentalis Cresson. Evolution, 53(2), 535-545.
Adams, D. C., & Church, J. O. (2008). Amphibians do not follow Bergmann's rule. Evolution, 62(2), 413-420. https://doi.org/10.1111/j.1558-5646.2007.00297.x
Aitchison, J. (1986). The statistical analysis of compositional data. Journal of the Royal Statistical Society, 44(2), 139-177. https://doi.org/10.1007/978-94-009-4109-0
Angilletta, M. J., Steury, T. D., & Sears, M. W. (2004). Temperature, growth rate, and body size in ectotherms: Fitting pieces of a life-history puzzle. Integrative and Comparative Biology, 44(6), 498-509. https://doi.org/10.1093/icb/44.6.498
Arbizu, M. (2017). Pairwise adonis: Pairwise multilevel comparison using adonis. R package version 0.0.1. Retrieved from https://github.com/pmartinezarbizu/pairwiseAdonis
Arnett, A. E., & Gotelli, N. J. (1999). Bergmann's rule in the ant lion Myrmeleon immaculatus DeGeer (Neuroptera: Myrmeleontidae): Geographic variation in body size and heterozygosity. Journal of Biogeography, 26(2), 275-283. https://doi.org/10.1046/j.1365-2699.1999.00271.x
Ashton, K. G., Tracy, M. C., & de Queiroz, A. (2000). Is Bergmann's rule valid for mammals? The American Naturalist, 156(4), 390-415. https://doi.org/10.1086/303400
Atkinson, D., & Sibly, R. M. (1997). Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends in Ecology & Evolution, 12, 235-239. https://doi.org/10.1016/S0169-5347(97)01058-6
Bartoń, K. (2016). MuMIn: Multi-model inference. R package version 1.15.6. Version, 1, 18. citeulike:11961261
Bates, D., Maechler, M., Bolker, B. M., & Walker, S. (2014). Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1-48. https://doi.org/10.18637/jss.v067.i01
Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological), 57(1), 289-300. https://doi.org/10.1111/j.2517-6161.1995.tb02031.x
Bernadou, A., Römermann, C., Gratiashvili, N., & Heinze, J. (2016). Body size but not colony size increases with altitude in the holarctic ant, Leptothorax acervorum. Ecological Entomology, 41(6), 733-736. https://doi.org/10.1111/een.12338
Bernays, E. A. (1991). Evolution of insect morphology in relation to plants. Philosophical Transactions - Royal Society of London B: Biological Sciences, 333(1267), 257-264. https://doi.org/10.1098/rstb.1991.0075
Bishop, T. R., Robertson, M. P., Gibb, H., van Rensburg, B. J., Braschler, B., Chown, S. L., … Parr, C. L. (2016). Ant assemblages have darker and larger members in cold environments. Global Ecology and Biogeography, 25(12), 1489-1499. https://doi.org/10.1111/geb.12516
Blanckenhorn, W. U. (2018). Adaptive phenotypic plasticity in growth, development, and body size in the yellow dung fly. Ecography, 52(525), 1394-1407.
Blanckenhorn, W. U., & Demont, M. (2004). Bergmann and converse bergmann latitudinal clines in arthropods: Two ends of a continuum? Integrative and Comparative Biology, 44(6), 413-424. https://doi.org/10.1093/icb/44.6.413
Blanckenhorn, W. U., & Fairbairn, D. J. (1995). Life history adaptation along a latitudinal cline in the water strider Aquarius remigis (Heteroptera: Gerridae). Journal of Evolutionary Biology, 8(1), 21-41. https://doi.org/10.1046/j.1420-9101.1995.8010021.x
Brassard, F., Francoeur, A., & Lessard, J.-P. (2020). Data from: Temperature drives caste-specific morphological clines in ants. Dryad Digital Repository, https://doi.org/10.5061/dryad.dncjsxkx3
Brown, J. H. (2014). Why are there so many species in the tropics? Journal of Biogeography, 41, 8-22. https://doi.org/10.1111/jbi.12228
Buschinger, A. (2009). Social parasitism among ants: A review (Hymenoptera: Formicidae). Myrmecological News, 12, 219-235.
Calabi, P., & Porter, S. D. (1989). Worker longevity in the fire ant Solenopsis invicta: Ergonomic considerations of correlations between temperature, size and metabolic rates. Journal of Insect Physiology, 35(8), 643-649. https://doi.org/10.1016/0022-1910(89)90127-3
Cerdá, X., Retana, J., & Cerda, X. (1997). Links between worker polymorphism and thermal biology in a thermophilic ant species. Oikos, 78(3), 467-474. https://doi.org/10.2307/3545608
Chatterjee, S., & Hadi, A. S. (2006). Regression diagnostics: Detection of model violations. In Regression analysis by example (pp. 85-120). Hoboken, NJ: John Wiley & Sons. https://doi.org/10.1002/0470055464.ch4
Chown, S. L., & Gaston, K. J. (2010). Body size variation in insects: A macroecological perspective. Biological Reviews, 85(1), 139-169. https://doi.org/10.1111/j.1469-185X.2009.00097.x
Chown, S. L., & Klok, C. J. (2003). Altitudinal body size clines: Latitudinal effects associated with changing seasonality. Ecography, 26(4), 445-455. https://doi.org/10.1034/j.1600-0587.2003.03479.x
Couzin, I. D., & Franks, N. R. (2002). Self-organized lane formation and optimized traffic flow in army ants. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(September), 139-146. https://doi.org/10.1098/rspb.2002.2210
Creighton, W. S. (1950). The ants of North America. Bulletin of the Museum of Comparative Zoology at Harvard College, 104, 1-585.
Cushman, J. H., Lawton, J. H., & Manly, B. F. J. (1993). Latitudinal patterns in European ant assemblages: Variation in species richness and body size. Oecologia, 95, 30-37. https://doi.org/10.1007/BF00649503
Davidson, D. W. (1982). Sexual selection in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex). Behavioral Ecology and Sociobiology, 10(4), 245-250. https://doi.org/10.1007/BF00302813
Davidson, D. W., Cook, S. C., & Snelling, R. R. (2004). Liquid-feeding performances of ants (Formicidae): Ecological and evolutionary implications. Oecologia, 139(2), 255-266. https://doi.org/10.1007/s00442-004-1508-4
Economo, E. P., Klimov, P., Sarnat, E. M., Guénard, B., Weiser, M. D., Lecroq, B., & Lacey Knowles, L. (2014). Global phylogenetic structure of the hyperdiverse ant genus Pheidole reveals the repeated evolution of macroecological patterns. Proceedings of the Royal Society B: Biological Sciences, 282(1798). https://doi.org/10.1098/rspb.2014.1416
Farji-Brener, A. G., Barrantes, G., & Ruggiero, A. (2004). Environmental rugosity, body size and access to food: A test of the size-grain hypothesis in tropical litter ants. Oikos, 104(1), 165-171. https://doi.org/10.1111/j.0030-1299.2004.12740.x
Fjerdingstad, E. J., & Boomsma, J. J. (1997). Variation in size and sperm content of sexuals in the leafcutter ant Atta colombica. Insectes Sociaux, 44(3), 209-218. https://doi.org/10.1007/s000400050042
Francoeur, A. (1973). Révision Taxonomique des espèces néarctiques du groupe fusca, genre Formica (Formicidae, Hymenoptera). Mémoires de La Société Entomologique Du Québec, 3, 1-312.
Geraghty, M. J., Dunn, R. R., & Sanders, N. J. (2007). Body size, colony size, and range size in ants (Hymenoptera: Formicidae): Are patterns along elevational and latitudinal gradients consistent with Bergmann's Rule? Myrmecological News, 10(September), 51-58.
Gibb, H., Sanders, N. J., Dunn, R. R., Arnan, X., Vasconcelos, H. L., Donoso, D. A., … Parr, C. L. (2018). Habitat disturbance selects against both small and large species across varying climates. Ecography, 41(7), 1184-1193. https://doi.org/10.1111/ecog.03244
Gillman, L. N., Wright, S. D., Cusens, J., Mcbride, P. D., Malhi, Y., & Whittaker, R. J. (2015). Latitude, productivity and species richness. Global Ecology and Biogeography, 24, 107-117. https://doi.org/10.1111/geb.12245
Gotelli, N. J., & Ellison, A. (2004). A primer of ecological statistics. The American Statistician, 59(4), 350. https://doi.org/10.1198/tas.2005.s32
Heinze, J. (1993). Life histories of subarctic ants. Arctic, 46(4), 354-358. https://doi.org/10.14430/arctic1363
Heinze, J., Foitzik, S., & Fischer, B. (2003). The significance of latitudinal variation in body size in a holarctic ant, Leptothorax acervorum. Ecography, 26(3), 349-355. https://doi.org/10.1034/j.1600-0587.2003.03478.x
Heinze, J., & Rueppell, O. (2014). The frequency of multi-queen colonies increases with altitude in a Nearctic ant. Ecological Entomology, 39(4), 527-529. https://doi.org/10.1111/een.12119
Helms, J. A. (2018). The flight ecology of ants (Hymenoptera: Formicidae). Myrmecological News, 26, 19-30.
Helms, J. A., & Godfrey, A. (2016). Dispersal polymorphisms in invasive fire ants. PLoS ONE, 11(4), e0153955. https://doi.org/10.1371/journal.pone.0153955
Herrel, A., Meyers, J. J., & Vanhooydonck, B. (2001). Correlations between habitat use and body shape in a phrynosomatid lizard (Urosaurus ornatus): A population-level analysis. Biological Journal of the Linnean Society, 74, 305-314. https://doi.org/10.1006/bijl.2001.0579
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). WorldClim. International Journal of Climatology, 25, 1965-1978. https://doi.org/10.1002/joc.1276
Hölldobler, B., & Bartz, S. H. (1985). Sociobiology of reproduction in ants. Fortschritte Der Zoologie, 31, 237-257.
Hölldobler, B., & Wilson, E. O. (2009). The superorganism (Vol. 456). New York, NY: W. W. Norton. https://doi.org/10.1038/456320a
Huang, M. H. (2010). Multi-phase defense by the big-headed ant, Pheidole obtusospinosa, against raiding army ants. Journal of Insect Science (Online), 10(1), 1-10. https://doi.org/10.1673/031.010.0101
Jeanne, R. L. (1979). A latitudinal gradient in rates of ant predation. Ecology, 60(6), 1211. https://doi.org/10.2307/1936968
Jílková, V., Cajthaml, T., & Frouz, J. (2015). Respiration in wood ant (Formica aquilonia) nests as affected by altitudinal and seasonal changes in temperature. Soil Biology and Biochemistry, 86, 50-57. https://doi.org/10.1016/j.soilbio.2015.03.024
Kadochová, Š., & Frouz, J. (2013). Thermoregulation strategies in ants in comparison to other social insects, with a focus on red wood ants (Formica rufa group). F1000Research, 2, 280. https://doi.org/10.12688/f1000research.2-280.v2
Kannowski, P. B., & Johnson, R. L. (1969). Male patrolling behaviour and sex attraction in ants of the genus Formica. Animal Behaviour, 3472(69), 425-429. https://doi.org/10.1016/0003-3472(69)90142-0
Kaspari, M. (1996). Worker size and seed size selection by harvester ants in a neotropical forest. Oecologia, 105(3), 397-404. https://doi.org/10.1007/BF00328743
Kaspari, M. (2005). Global energy gradients and size in colonial organisms: Worker mass and worker number in ant colonies. Proceedings of the National Academy of Sciences of the United States of America, 102(14), 5079-5083. https://doi.org/10.1073/pnas.0407827102
Kaspari, M., Clay, N. A., Lucas, J., Yanoviak, S. P., & Kay, A. (2015). Thermal adaptation generates a diversity of thermal limits in a rainforest ant community. Global Change Biology, 21(3), 1092-1102. https://doi.org/10.1111/gcb.12750
Kaspari, M., & Weiser, M. D. (1999). The size-grain hypothesis and interspecific scaling in ants. Functional Ecology, 13(4), 530-538. https://doi.org/10.1046/j.1365-2435.1999.00343.x
Keller, R. A., Peeters, C., & Beldade, P. (2014). Evolution of thorax architecture in ant castes highlights trade-off between flight and ground behaviors. eLife, 2014(3), 01539. https://doi.org/10.7554/eLife.01539
Kipyatkov, V. E. (1993). Annual cycles of development in ants: Diversity, evolution, regulation. Proceedings of the Colloquia on Social Insects, 2, 25-48.
Kivelä, S. M., Välimäki, P., Carrasco, D., Mäenpää, M. I., & Oksanen, J. (2011). Latitudinal insect body size clines revisited: A critical evaluation of the saw-tooth model. Journal of Animal Ecology, 80(6), 1184-1195. https://doi.org/10.1111/j.1365-2656.2011.01864.x
Klingenberg, C. P. (2016). Size, shape, and form: Concepts of allometry in geometric morphometrics. Development Genes and Evolution, 226(3), 113-137. https://doi.org/10.1007/s00427-016-0539-2
Koehl, M. A. R. (1996). When does morphology matter? Annual Review of Ecology and Systematics, 27, 501-542. https://doi.org/10.1146/annurev.ecolsys.27.1.501
Legendre, P., & Andersson, M. J. (1999). Distance-based redundancy analysis: Testing multispecies responses in multifactorial ecological experiments. Ecological Monographs, 69(1), 1-24. https://doi.org/10.1890/0012-9615(1999)069[0001:DBRATM]2.0.CO;2
Losos, J. B. (1990a). Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: An evolutionary analysis. Ecological Monographs, 60, 369-388. https://doi.org/10.2307/1943062
Losos, J. B. (1990b). The evolution of form and function: Morphology and locomotor performance in West Indian Anolis lizards. Evolution, 44(5), 1189-1203. https://doi.org/10.1111/j.1558-5646.1990.tb05225.x
Masaki, S. (1967). Geographic variation and climatic adaptation in a field cricket (Orthoptera: Gryllidae). Evolution, 21(4), 725-741. https://doi.org/10.2307/2406770
Mazerolle, M. J. (2015). Package ‘AICcmodavg’. R Environment, (c), 1-141.
Mccaffrey, J., & Galen, C. (2011). Between a rock and a hard place: Impact of nest selection behavior on the altitudinal range of an Alpine ant, Formica neorufibarbis. Environmental Entomology, 40(3), 534-540. https://doi.org/10.1603/en10304
McGill, B. J., Enquist, B. J., Weiher, E., & Westoby, M. (2006). Rebuilding community ecology from functional traits. Trends in Ecology & Evolution, 21(4), 178-185. https://doi.org/10.1016/j.tree.2006.02.002
Meiri, S., & Dayan, T. (2003). On the validity of Bergmann's rule. Journal of Biogeography, 30(3), 331-351. https://doi.org/10.1046/j.1365-2699.2003.00837.x
Molet, M., Péronnet, R., Couette, S., Canovas, C., & Doums, C. (2017). Effect of temperature and social environment on worker size in the ant Temnothorax nylanderi. Journal of Thermal Biology, 67, 22-29. https://doi.org/10.1016/j.jtherbio.2017.04.013
Mori, A., & Moli, F. L. (1998). Mating behavior and colony founding of the slave-making ant Formica sanguinea (Hymenoptera: Formicidae). Journal of Insect Behavior, 11, 235-245. https://doi.org/10.1023/A:1021048024219
Narendra, A., Reid, S. F., Greiner, B., Peters, R. A., Hemmi, J. M., Ribi, W. A., & Zeil, J. (2011). Caste-specific visual adaptations to distinct daily activity schedules in Australian Myrmecia ants. Proceedings of the Royal Society B: Biological Sciences, 278(1709). https://doi.org/10.1098/rspb.2010.1378
Nogueira, M. R., Peracchi, A. L., & Monteiro, L. R. (2009). Morphological correlates of bite force and diet in the skull and mandible of phyllostomid bats. Functional Ecology, 23, 715-723. https://doi.org/10.1111/j.1365-2435.2009.01549.x
Ohkawara, K., Nakamura, K., Kadokura, N., & Terashita, T. (2017). Geographical variation in mandible morphologies specialised for collembolan predation depend on prey size in the ant Strumigenys lewisi. Ecological Entomology, 42(2), 156-163. https://doi.org/10.1111/een.12374
Oksanen, J., Blanchet, F. G., Friendly, M., Kindt, R., Legendre, P., Mcglinn, D., & Wagner, H. (2016). Vegan: Community ecology package. Retrieved from https://cran.r-project.org; https://github.com/vegandevs/vegan
Olson, V. A., Davies, R. G., Orme, C. D. L., Thomas, G. H., Meiri, S., Blackburn, T. M., … Bennett, P. M. (2009). Global biogeography and ecology of body size in birds. Ecology Letters, 12(3), 249-259. https://doi.org/10.1111/j.1461-0248.2009.01281.x
Oms, C. S., Cerdá, X., & Boulay, R. (2017). Is phenotypic plasticity a key mechanism for responding to thermal stress in ants? The Science of Nature, 104(5-6), 5-6. https://doi.org/10.1007/s00114-017-1464-6
O'Neill, K. M. (1994). The male mating strategy of the ant Formica subpolita Mayr (Hymenoptera: Formicidae): Swarming, mating, and predation risk. Psyche: A Journal of Entomology, 101(1-2), 93-108. https://doi.org/10.1155/1994/38217
Oster, G. F., & Wilson, E. O. (1978). Caste and ecology in the social insects (Vol. 12). Princeton, NJ: Princeton University.
Paul, J. (2001). Mandible movements in ants. Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology, 131(1), 7-20. https://doi.org/10.1016/S1095-6433(01)00458-5
Peeters, C. (2012). Convergent evolution of wingless reproductives across all subfamilies of ants, and sporadic loss of winged queens (Hymenoptera: Formicidae). Myrmecological News, 16, 75-91.
Penick, C. A., Diamond, S. E., Sanders, N. J., & Dunn, R. R. (2017). Beyond thermal limits: Comprehensive metrics of performance identify key axes of thermal adaptation in ants. Functional Ecology, 31(5), 1091-1100. https://doi.org/10.1111/1365-2435.12818
Peres-Neto, P. R., & Magnan, P. (2004). The influence of swimming demand on phenotypic plasticity and morphological integration: A comparison of two polymorphic charr species. Oecologia, 140(1), 36-45. https://doi.org/10.1007/s00442-004-1562-y
Pinkert, S., Brandl, R., & Zeuss, D. (2017). Colour lightness of dragonfly assemblages across North America and Europe. Ecography, 40(9), 1110-1117. https://doi.org/10.1111/ecog.02578
Pollock, L. J., Morris, W. K., & Vesk, P. A. (2012). The role of functional traits in species distributions revealed through a hierarchical model. Ecography, 35(8), 716-725. https://doi.org/10.1111/j.1600-0587.2011.07085.x
Porter, S. D. (1988). Impact of temperature on colony growth and developmental rates of the ant, Solenopsis invicta. Journal of Insect Physiology, 34(12), 1127-1133. https://doi.org/10.1016/0022-1910(88)90215-6
Powell, S. (2008). Ecological specialization and the evolution of a specialized caste in Cephalotes ants. Functional Ecology, 22(5), 902-911. https://doi.org/10.1111/j.1365-2435.2008.01436.x
Powell, S. (2009). How ecology shapes caste evolution: Linking resource use, morphology, performance and fitness in a superorganism. Journal of Evolutionary Biology, 22, 902-911. https://doi.org/10.1111/j.1420-9101.2009.01710.x
Powell, S., & Franks, N. R. (2006). Ecology and the evolution of worker morphological diversity: A comparative analysis with Eciton army ants. Functional Ecology, 20(6), 1105-1114. https://doi.org/10.1111/j.1365-2435.2006.01184.x
Price, P. W., Diniz, I. R., Morais, H. C., & Marques, E. S. A. (1995). The abundance of insect herbivore species in the tropics: The high local richness of rare species. Biotropica, 27(4), 468. https://doi.org/10.2307/2388960
Purcell, J., Pirogan, D., Avril, A., Bouyarden, F., & Chapuisat, M. (2016). Environmental influence on the phenotype of ant workers revealed by common garden experiment. Behavioral Ecology and Sociobiology, 70(3), 357-367. https://doi.org/10.1007/s00265-015-2055-1
QGIS Development Team. (2015). QGIS geographic information system. Open Source Geospatial Foundation Project. Retrieved from http://www.qgis.org/
R Core Team. (2017). R: A language and environment for statistical computing (Vol. 55, pp. 275-286). R Development Core Team. Retrieved from http://www.R-project.org
Romiguier, J., Rolland, J., Morandin, C., & Keller, L. (2018). Phylogenomics of palearctic Formica species suggests a single origin of temporary parasitism and gives insights to the evolutionary pathway toward slave-making behaviour. BMC Evolutionary Biology, 18(1), 40-48. https://doi.org/10.1186/s12862-018-1159-4
Roslin, T., Hardwick, B., Novotny, V., Petry, W. K., Andrew, N. R., Asmus, A., … Slade, E. M. (2017). Latitudinal gradients: Higher predation risk for insect prey at low latitudes and elevations. Science, 356(6339), 742-744. https://doi.org/10.1126/science.aaj1631
Rüppell, O., & Heinze, J. (1999). Alternative reproductive tactics in females: The case of size polymorphism in winged ant queens. Insectes Sociaux, 46(1), 6-17. https://doi.org/10.1007/s000400050106
Salewski, V., & Watt, C. (2017). Bergmann's rule: A biophysiological rule examined in birds. Oikos, 126(2), 03698. https://doi.org/10.1111/oik.03698
Sarnat, E. M., Friedman, N. R., Fischer, G., Lecroq-Bennet, B., & Economo, E. P. (2017). Rise of the spiny ants: Diversification, ecology and function of extreme traits in the hyperdiverse genus Pheidole (Hymenoptera: Formicidae). Biological Journal of the Linnean Society, 122(3), 514-538. https://doi.org/10.1093/biolinnean/blx081
Schemske, D. W., Mittelbach, G. G., Cornell, H. V., Sobel, J. M., & Roy, K. (2009). Is there a latitudinal gradient in the importance of biotic interactions? Annual Review of Ecology, Evolution, and Systematics, 40(1), 245-269. https://doi.org/10.1146/annurev.ecolsys.39.110707.173430
Schöning, C., Kinuthia, W., & Franks, N. R. (2005). Evolution of allometries in the worker caste of Dorylus army ants. Oikos, 110(2), 231-240. https://doi.org/10.1111/j.0030-1299.2005.13672.x
Schluter, D. (1993). Adaptive radiation in sticklebacks: Size, shape, and habitat use efficiency. Ecology, 74, 699-709. https://doi.org/10.2307/1940797
Schutze, M. K., & Clarke, A. R. (2008). Converse bergmann cline in a Eucalyptus herbivore, Paropsis atomaria Olivier (Coleoptera: Chrysomelidae): Phenotypic plasticity or local adaptation? Global Ecology and Biogeography, 17(3), 424-431. https://doi.org/10.1111/j.1466-8238.2007.00374.x
Shelomi, M. (2012). Where are we now? Bergmann's rule sensu lato in insects. The American Naturalist, 180(4), 511-519. https://doi.org/10.1086/667595
Shik, J. Z., Arnan, X., Oms, C. S., Cerdá, X., & Boulay, R. (2019). Evidence for locally adaptive metabolic rates among ant populations along an elevational gradient. Journal of Animal Ecology, 88(8), 1240-1249. https://doi.org/10.1111/1365-2656.13007
Shik, J. Z., Donoso, D. A., & Kaspari, M. (2013). The life history continuum hypothesis links traits of male ants with life outside the nest. Entomologia Experimentalis et Applicata, 149(2), 99-109. https://doi.org/10.1111/eea.12117
Stillwell, R. C., Morse, G. E., & Fox, C. W. (2007). Geographic variation in body size and sexual size dimorphism of a seed-feeding beetle. The American Naturalist, 170(3), 358-369. https://doi.org/10.1086/520118
Stürup, M., den Boer, S. P. A., Nash, D. R., Boomsma, J. J., & Baer, B. (2011). Variation in male body size and reproductive allocation in the leafcutter ant Atta colombica: Estimating variance components and possible trade-offs. Insectes Sociaux, 58(1), 47-55. https://doi.org/10.1007/s00040-010-0115-0
Sunday, J. M., Bates, A. E., Kearney, M. R., Colwell, R. K., Dulvy, N. K., Longino, J. T., & Huey, R. B. (2014). Thermal-safety margins and the necessity of thermoregulatory behavior across latitude and elevation. Proceedings of the National Academy of Sciences of the United States of America. 111(15), 5610-5615. https://doi.org/10.1073/pnas.1316145111
Sundström, L. (1995). Dispersal polymorphism and physiological condition of males and females in the ant, Formica truncorum. Behavioral Ecology, 6(2), 132-139. https://doi.org/10.1093/beheco/6.2.132
Swenson, N. G., & Weiser, M. D. (2010). Plant geography upon the basis of functional traits: An example from eastern North American trees. Ecology, 91(8), 2234-2241. https://doi.org/10.1890/09-1743.1
Thuiller, W., Lavorel, S., Midgley, G., Lavergne, S., & Rebelo, T. (2004). Relating plant traits and species distributions along bioclimatic gradients for 88 Leucadendron taxa. Ecology, 85(6), 1688-1699. https://doi.org/10.1890/03-0148
Tiede, Y., Hemp, C., Schmidt, A., Nauss, T., Farwig, N., & Brandl, R. (2018). Beyond body size: Consistent decrease of traits within orthopteran assemblages with elevation. Ecology, 99(9), 2090-2102. https://doi.org/10.1002/ecy.2436
Trible, W., & Kronauer, D. J. C. (2017). Caste development and evolution in ants: It's all about size. The Journal of Experimental Biology, 220(1), 53-62. https://doi.org/10.1242/jeb.145292
Vargo, E. L., & Fletcher, D. J. C. (1989). On the relationship between queen number and fecundity in polygyne colonies of the fire ant Solenopsis invicta. Physiological Entomology, 14, 223-232. https://doi.org/10.1111/j.1365-3032.1989.tb00955.x
Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., & Garnier, E. (2007). Let the concept of trait be functional! Oikos, 116, 882-892. https://doi.org/10.1111/j.0030-1299.2007.15559.x
Vitikainen, E. I. K., Haag-Liautard, C., & Sundström, L. (2015). Natal dispersal, mating patterns, and inbreeding in the ant formica exsecta. The American Naturalist, 186(6), 716-727. https://doi.org/10.1086/683799
Weiser, M. D., & Kaspari, M. (2006). Ecological morphospace of new world ants. Ecological Entomology, 31(2), 131-142. https://doi.org/10.1111/j.0307-6946.2006.00759.x
Wiernasz, D. C., & Cole, B. J. (2003). Queen size mediates queen survival and colony fitness in harvester ants. Evolution; International Journal of Organic Evolution, 57(9), 2179-2183. https://doi.org/10.1111/j.0014-3820.2003.tb00396.x
Wiernasz, D. C., Sater, A. K., Abell, A. J., & Cole, B. J. (2001). Male size, sperm transfer, and colony fitness in the western harvester ant, Pogonomyrmex occidentals. Evolution, 55(2), 324-329. https://doi.org/10.1111/j.0014-3820.2001.tb01297.x
Wootton, R. (1992). Functional morphology of insect wings. Annual Review of Entomology, 37, 113-140. https://doi.org/10.1146/annurev.ento.37.1.113