Limited sex differences in plastic responses suggest evolutionary conservatism of thermal reaction norms: A meta-analysis in insects
Status PubMed-not-MEDLINE Jazyk angličtina Země Velká Británie, Anglie Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
36579171
PubMed Central
PMC9783480
DOI
10.1002/evl3.299
PII: EVL3299
Knihovny.cz E-zdroje
- Klíčová slova
- Body size, development rate, evolutionary constraint, growth rate, sexual bimaturism, sexual size dimorphism, thermal sensitivity, thermal trait,
- Publikační typ
- časopisecké články MeSH
Temperature has a profound effect on the growth and development of ectothermic animals. However, the extent to which ecologically driven selection pressures can adjust thermal plastic responses in growth schedules is not well understood. Comparing temperature-induced plastic responses between sexes provides a promising but underexploited approach to evaluating the evolvability of thermal reaction norms: males and females share largely the same genes and immature environments but typically experience different ecological selection pressures. We proceed from the idea that substantial sex differences in plastic responses could be interpreted as resulting from sex-specific life-history optimization, whereas similarity among the sexes should rather be seen as evidence of an essential role of physiological constraints. In this study, we performed a meta-analysis of sex-specific thermal responses in insect development times, using data on 161 species with comprehensive phylogenetic and ecological coverage. As a reference for judging the magnitude of sex specificity in thermal plasticity, we compared the magnitude of sex differences in plastic responses to temperature with those in response to diet. We show that sex-specific responses of development times to temperature variation are broadly similar. We also found no strong evidence for sex specificity in thermal responses to depend on the magnitude or direction of sex differences in development time. Sex differences in temperature-induced plastic responses were systematically less pronounced than sex differences in responses induced by variations in larval diet. Our results point to the existence of substantial constraints on the evolvability of thermal reaction norms in insects as the most likely explanation. If confirmed, the low evolvability of thermal response is an essential aspect to consider in predicting evolutionary responses to climate warming.
Zobrazit více v PubMed
Abdelrahman, I. 1974. Growth, development and innate capacity for increase in
Ahmadi, K. , Sengonca C., and Blaeser P. 2007. Effect of two different temperatures on the biology of predatory flower bug
Ahn, J. J. , Choi K. S., and Koh S. 2019. Effects of temperature on the development, fecundity, and life table parameters of
Alcalay, Y. , Puzhevsky D., Tsurim I., Scharf I., and Ovadia O. 2018. Interactive and sex‐specific life‐history responses of
Allsopp, P. G. 1977. Biology and capacity for increase of
Allsopp, P. G. , Cowie B. A., and Franzmann B. A. 1983. Development of immature stages of the lucerne leafroller
Amano, K. 1983. Studies on the intraspecific competition in dung‐breeding flies I. Effects of larval density on yellow dung fly,
Amin, O. M. , Jun L., Shangjun L., Yumei Z., and Liannzhi S. 1993. Development and longevity of PubMed
Amoudi, M. A. 1993. Effect of temperature on the developmental stages of PubMed
Arakawa, R. , and Namura Y. 2002. Effects of temperature on development of three
Armbruster, P. , and Conn J. E. 2006. Geographic variation of larval growth in North American
Atwal, A. S. 1955. Influence of temperature, photoperiod, and food on the speed of development, longevity, fecundity, and other qualities of the diamond‐back moth
Barbosa, P. , Waldvogel M., Martinat P., and Douglass L. W. 1983. Developmental and reproductive performance of the gypsy moth,
Barbosa, P. , Martinat P., and Waldvogel M. 1986. Development, fecundity and survival of the herbivore
Bari, M. N. , Jahan M., and Islam K. S. 2015. Effects of temperature on the life table parameters of PubMed
Barker, J. E. , Poppy G. M., and Payne C. C. 2006. Suitability of Arabidopsis thaliana as a model for host plant–
Barzegar, S. , Zamani A. A., Abbasi S., Shooshtari R. V., and Farsani N. S. 2016. Temperature‐dependent development modeling of the phorid fly PubMed
Bauerfeind, S. S. , and Fischer K. 2005. Effects of food stress and density in different life stages on reproduction in a butterfly. Oikos. 111:514–524.
Bauerfeind, S. S. , and Fischer K. 2009. Effects of larval starvation and adult diet‐derived amino acids on reproduction in a fruit‐feeding butterfly. Entomol. Exp. Appl. 130:229–237.
Bavaresco, A. , Garcia M. S., Grützmacher A. D., and Ringenberg J. F. R. 2002. Biology and thermal requirements of
Bazzocchi, G. G. , Lanzoni A., Burgio G., and Fiacconi M. R. 2003. Effects of temperature and host on the pre‐imaginal development of the parasitoid
Bell, H. A. , Marris G. C., Smethurst F., and Edwards J. P. 2003. The effect of host stage and temperature on selected developmental parameters of the solitary endoparasitoid
Berner, D. , Blanckenhorn W. U., and Körner C. 2005. Grasshoppers cope with low host plant quality by compensatory feeding and food selection: N limitation challenged. Oikos. 111:525–533.
Bezerra, C. E. S. , Tavares P. K. A., Nogueira C. H. F., Macedo L. P. M., and Araujo E. L. 2012. Biology and thermal requirements of
Blanckenhorn, W. U. , and Henseler C. 2005. Temperature‐dependent ovariole and testis maturation in the yellow dung fly. Entomol. Exp. Appl. 116:159–165.
Blanckenhorn, W. U. 1997. Altitudinal life history variation in the dung flies PubMed
Blanckenhorn, W. U. 1997. Effects of temperature on growth, development and diapause in the yellow dung fly ‐ against all the rules? Oecologia. 111:318–324. PubMed
Blanckenhorn, W. U. , and Heyland A. 2004. The quantitative genetics of two life history trade‐offs in the yellow dung fly in abundant and limited food environments. Evol. Ecol. 18:385–402.
Bommireddy, P. L. , Parajulee M. N., and Porter D. O. 2004. Influence of constant temperatures on life history of immature
Bonte, J. , Vangansbeke D., Maes S., Bonte M., Conlong D., and De Clercq P. 2012. Moisture source and diet affect development and reproduction of PubMed PMC
Bonte, J. , De Ro M., Conlong D., and De Clercq P. 2012. Thermal biology of the predatory bugs
Brakefield, P. M. , and Mazzotta V. 1995. Matching field and laboratory environments: effects of neglecting daily temperature variation on insect reaction norms. J. Evol. Biol. 8:559–573.
Buei, K. , Park S. H., and Yamugi H. 1978. Bionomics of three species of fleshflies,
Burke, S. , Pullin A. S., Wilson R. J., and Thomas C. D. 2005. Selection for discontinuous life‐history traits along a continuous thermal gradient in the butterfly Aricia agestis. Ecol. Entomol. 30:613–619.
Cave, R. D. , Sciacchetano C., and Diaz R. 2009. Temperature‐dependent development of the cycad aulacaspis scale,
Charles, J. G. , Kean J. M., and Chhagan A. 2006. Developmental parameters and voltinism of the painted apple moth,
Chen, C. , Xia Q. ‐ W., Xiao H. ‐ J., Xiao L., and Xue F. ‐ S. 2014. A comparison of the life‐history traits between diapause and direct development individuals in the cotton bollworm, PubMed PMC
Chong, J. ‐ H. , Oetting R. D., and van Iersel M. W. 2003. Temperature effects on the development, survival, and reproduction of the Madeira mealybug,
Chong, J. ‐ H. , Roda A. L., and Mannion C. M. 2008. Life history of the mealybug, PubMed
Combs, R. L. , and Valerio J. R. 1980. Biology of the fall armyworm on four varieties of bermudagrass when held at constant temperatures. Environ. Entomol. 9:393–396.
Silva, C. A. D. 2004. Efeitos da temperatura no desenvolvimento, fecundidade e longevidade de
De Block, M. , and Stoks R. 2003. Adaptive sex‐specific life history plasticity to temperature and photoperiod in a damselfly. J. Evol. Biol. 16:986–995. PubMed
Del Pino, M. , Cabello T., and Hernandez‐Suarez E. 2020. Age‐stage, two‐sex life table of PubMed
Diamond, S. E. , and Kingsolver J. G. 2010. Environmental dependence of thermal reaction norms: host plant quality can reverse the temperature‐size rule. Am. Nat. 175:1–10. PubMed
Doganlar, O. 2008. Temperature‐dependent development and degree‐day model of European leaf roller,
Farjana, T. , Tuno N., and Higa Y. 2012. Effects of temperature and diet on development and interspecies competition in PubMed
Farsani, N. S. , Zamani A. A., Abbasi S., and Kheradmand K. 2013. Effect of temperature and button mushroom varieties on life history of PubMed
Ferreira de Almeida, M. A. , Pires do Prado A., and Geden C. J. 2002. Influence of temperature on development time and longevity of
Fischer, K. , and Fiedler K. 2000. Sex‐related differences in reaction norms in the butterfly
Fischer, K. , and Fiedler K. 2000. Response of the copper butterfly PubMed
Fischer, K. , and Fiedler K. 2001. Dimorphic growth patterns and sex‐specific reaction norms in the butterfly
Fischer, K. , and Fiedler K. 2002. Reaction norms for age and size at maturity in response to temperature: a test of the compound interest hypothesis. Evol. Ecol. 16:333–349.
Fischer, K. , Brakefield P. M., and Zwaan B. J. 2003. Plasticity in butterfly egg size: why larger offspring at lower temperatures? Ecology. 84:3138–3147.
Folgarait, P. J. , Chirino M. G., Wilson Patrock R. J., and Gilbert L. E. 2005. Development of PubMed
Forsberg, J. , and Wiklund C. 1988. Protandry in the green‐veined white butterfly,
Francis, A. W. , Kairo M. T. K., and Roda A. L. 2012. Developmental and reproductive biology of
Frouz, J. , Ali A., and Lobinske R. J. 2002. Influence of temperature on developmental rate, wing length, and larval head capsule size of pestiferous midge PubMed
Fukuda, T. , Wakamura S., Arakaki N., and Yamagishi K. 2007. Parasitism, development and adult longevity of the egg parasitoid PubMed
Gautam, S. G. , Opit G. P., and Giles K. L. 2010. Population growth and development of the psocid PubMed
Gautam, S. G. , Opit G. P., and Shakya K. 2016. Population growth and development of the psocid PubMed
Geden, C. J. , Ferreira de Almeida M. A., and Pires do Prado A. 2003. Effects of Nosema disease on fitness of the parasitoid
Gillespie, D. R. , and McGregor R. R. 2000. The functions of plant feeding in the omnivorous predator
Gillespie, D. R. , Sanchez J. A. S., and McGregor R. R. 2004. Cumulative temperature requirements and development thresholds in two populations of
Golizadeh, A. , and Zalucki M. P. 2012. Estimating temperature‐dependent developmental rates of potato tuberworm,
Gomi, T. 2006. Sexual difference in the effect of temperature on the larval development in
Gotoh, T. , Koyama M., Hagino Y., and Doke K. 2011. Effect of leaf toughness and temperature on development in the lilac pyralid,
Graeve, I. 2008. Degree days and phenological synchrony in Western tussock moth and coast live oak. Master's thesis, San Jose State University, San Jose, CA.
Greenberg, S. M. , Setamou M., Sappington T. W., Liu T. ‐ X., Coleman R. J., and Armostrong J. S. 2005. Temperature‐dependent development and reproduction of the boll weevil (Coleoptera: Curculionidae). Insect Science. 12:449–459.
Guzman, L. I. , and Frake A. M. 2007. Temperature affects
Hamilton, J. G. , and Zalucki M. P. 1991. Effect of temperature on development rate, survival and fecundity of cotton tipworm,
Hamilton, J. G. , and Zalucki M. P. 1993. Interactions between a specialist herbivore,
Harries, F. H. , and Douglass J. R. 1948. Bionomic studies on the beet leafhopper. Ecol. Monogr. 18:45–79.
He, X. , Wang Q., and Carpenter A. 2003. Thermal requirements for the development and reproduction of PubMed
Hill, J. K. , and Gatehouse A. G. 1992. Effects of temperature and photoperiod on development and pre‐reproductive period of the silver Y moth
Hoang, L. K. , and Takasu K. 2005. Helicoverpa armigera as an alternative host of the larval parasitoid
Hoddle, M. S. 2002. Developmental and reproductive biology of PubMed
Horgan, F. G. , Quiring D. T., Lagnaoui A., and Pelletier Y. 2012. Life histories and fitness of two tuber moth species feeding on native Andean potatoes. Neotrop. Entomol. 41:333–340. PubMed
Horgan, F. G. , Quiring D. T., Lagnaoui A., Salas A. R., and Pelletier Y. 2007. Periderm‐ and cortex‐based resistance to tuber‐feeding
Hou, Y. , and Weng Z. 2010. Temperature‐dependent development and life table parameters of PubMed
Huang, X. ‐ L. , Xiao L., he H. ‐ M., and Xue F. ‐ S. 2018. Effect of rearing conditions on the correlation between larval development time and pupal weight of the rice stem borer, PubMed PMC
Ichiki, R. , and Nakamura S. 2007. Oviposition and immature development of the parasitoid fly
Ichiki, R. , Takasu K., and Shima H. 2003. Effects of temperature on immature development of the parasitic fly
Iltis, C. , Louapre P., Pecharova K., Thiery D., Zito S., Bois B., et al. 2019. Are life‐history traits equally affected by global warming? A case study combining a multi‐trait approach with fine‐grain climate modeling. J. Insect Physiol. 117:103916. PubMed
Ishijima, C. , Sato Y., and Ohtaishi M. 2008. Effect of temperature and host on the development, sex ratio, emergence rate and body size of
Jang, T. , Rho M. S., Koh S. ‐ H., and Lee K. P. 2015. Host–plant quality alters herbivore responses to temperature: a case study using the generalist
Johnson, T. , and Giliomee J. H. 2011. Development of the oleander mealybug,
Jones, J. M. , and Stephen F. M. 1994. Effect of temperature on development of hymenopterous parasitoids of
Joseph, G. , and Kelsey R. G. 1994. Acceptability and suitability of douglas‐fir as a secondary host for gypsy moth (Lepidoptera: Lymantriidae). Environ. Entomol. 23:396–405.
Kalaitzaki, A. P. , Lykouressis D. P., Perdikis D. C., and Alexandrakis V. Z. 2007. Effect of temperature on development and survival of the parasitoid PubMed
Karamaouna, F. , and Copland M. J. W. 2000. Host suitability, quality and host size preference of
Karamaouna, F. , and Copland M. J. 2009. Fitness and life history parameters of
Karolewski, P. , Grzebyta J., Oleksyn J., and Gietrych M. J. 2007. Temperature affects performance of
Kemmochi, T. , Fujimori S., and Saito T. 2016. The leafminer PubMed
Khan, M. , Gregg P., and Mensah R. 2009. Effect of temperature on the biology of
Kingsolver, J. G. , Ragland G. J., and Diamond S. E. 2009. Evolution in a constant environment: thermal fluctuations and thermal sensitivity of laboratory and field populations of PubMed
Kitajima, H. , Sakata H., Kunitomo S., and Kawashima Y. 2016. Effects of temperature on the development of
Kivan, M. , and Kilic N. 2006. Age‐specific fecundity and life table of
Kivelä, S. M. , Välimäki P., and Mäenpää M. I. 2012. Genetic and phenotypic variation in juvenile development in relation to temperature and developmental pathway in a geometrid moth. J. Evol. Biol. 25:881–891. PubMed
Krasnov, B. R. , Khoklova I. S., Fielden L. J., and Burdelova N. V. 2001. Development rates of two PubMed
Kruse, J. J. , and Raffa K. F. 1997. Effects of selected midwestern larval host plants on performance by two strains of the gypsy moth (Lepidoptera: Lymantriidae) parasitoid
Lance, D. R. , Elkinton J. S., and Schwalbe C. P. 1986. Feeding rhythms of gypsy moth larvae: effect of food quality during outbreaks. Ecology. 67:1650–1654.
Larios, G. L. B. , Ohno K., and Fukuhara F. 2007. Effects of photoperiod and temperature on preimaginal development and summer diapause of
Lauziere, I. , Setamou M., Legaspi J., and Jones W. 2002. Effect of temperature on the life cycle of
Lazarević, J. , Perić‐Mataruga V., Stojković B., and Tucić N. 2002. Adaptation of the gypsy moth to an unsuitable host plant. Entomol. Exp. Appl. 102:75–86.
Legaspi, J. C. , and Legaspi B. C. 2005. Life table analysis for
Legaspi, J. C. , Legaspi B. C., Simmons A. M., and Soumare M. 2008. Life table analysis for immatures and female adults of the predatory beetle, PubMed PMC
Lehtovaara, V. J. , Roininen H., and Valtonen A. 2018. Optimal temperature for rearing the edible PubMed
Lindroth, R. L. , Klein K. A., Hemming J. D. C., and Feuker A. M. 1997. Variation in temperature and dietary nitrogen affect performance of the gypsy moth (
Liu, Y. H. , and Tsai J. H. 2002. Effect of temperature on development, survivorship, and fecundity of
Liu, J. ‐ F. , Liu M., Yang M. ‐ F., Kontodimas D. C., Yu X. ‐ F., and Lian Q. ‐ X. 2014. Temperature‐dependent development of
Lopatina, E. B. , and Gusev I. A. 2019. A novel form of phenotypic plasticity of the thermal reaction norms for development in the bug
Luo, S. , Zhang F., and Wu K. 2015. Effect of temperature on the reproductive biology of
Lysyk, T. J. 2001. Relationships between temperature and life history parameters of
Lyytinen, A. , Lindström L., and Mappes J. 2008. Genetic variation in growth and development time under two selection regimes in
Mafi, S. , and Ohbayashi N. 2010. Biology of
Mahdian, K. , Kerckhove J., Tirry L., and De Clercq P. 2006. Effects of diet on development and reproduction of the predatory pentatomids
Mahmood, A. R. , Liu S. S., Shi Z. H., Song X. H., and Zalucki M. P. 2003. Lack of intraspecific biological variation between two geographical populations of PubMed
Malekmohammadi, A. , Shishehbor P., and Kocheili F. 2012. Influence of constant temperatures on development, reproduction and life table parameters of
Mao, H. , and Kunimi Y. 1990. Effects of temperature and photoperiod on development of the oriental tea tortrix
Mawela, K. V. , Kfir R., and Krüger K. 2013. Effect of temperature and host species on parasitism, development time and sex ratio of the egg parasitoid
McDonald, R. S. , and Borden J. H. 1995. Protandry in
Milonas, P. G. , and Savopoulou‐Soultani M. 2000. Development, survivorship, and reproduction of
Milosavljevic, I. , McCalla K. A., Ratkowsky D. A., and Hoddle M. S. 2019. Effects of constant and fluctuating temperatures on development rates and longevity of PubMed
Mirhosseini, M. A. , Fathipour Y., Soufbaf M., and Reddy G. V. P. 2018. Thermal requirements and development response to constant temperatures by PubMed
Mo, J. , Glover M., Munro S., and Beattie A. C. 2006. Development of PubMed
Morales‐Ramos, J. A. , and Rojas M. G. 2017. Temperature‐dependent biological and demographic parameters of PubMed PMC
Myers, H. M. , Tomberlin J. K., Lambert B. D., and Kattes D. 2008. Development of black soldier fly (Diptera: Stratiomyidae) larvae fed dairy manure. Environ. Entomol. 37:11–15. PubMed
Nabeta, F. H. , Nakai M., and Kunimi Y. 2005. Effects of temperature and photoperiod on the development and reproduction of
Nieuwenhove, G. A. , Frias E. A., and Virla E. G. 2016. Effects of temperature on the development, performance and fitness of the corn leafhopper
Noor‐ul‐Ane, M. , and Jung C. 2020. Temperature‐dependent development and survival of small hive beetle,
Ohta, I. 2001. Effect of temperature on development of
Okada, K. , and Miyatake T. 2007.
Ottenheim, M. M. , Volmer A. D., and Holloway G. J. 1996. The genetics of phenotypic plasticity in adult abdominal colour pattern of
Pakyari, H. , Fathipour Y., and Enkegaard A. 2011. Estimating development and temperature thresholds of
Pandey, S. , and Singh R. 1999. Host size induced variation in progeny sex ratio of an aphid parasitoid
Panizzi, A. R. 1992. Performance of
Pappas, M. L. , Karagiorgou E., Papaioannou G., Koveos D. S., and Broufas G. D. 2013. Developmental temperature responses of
Prasad, Y. G. , Prabhakar M., Sreedevi G., Ramachandra Rao G., and Venkateswarlu B. 2012. Effect of temperature on development, survival and reproduction of the mealybug,
Reed, D. A. , Ganjisaffar F., Palumbo J. C., and Perring T. M. 2017. Effects of temperatures on immature development and survival of the invasive stink bug PubMed
Rizvi, S. Z. M. , Raman A., Wheatley W. M., and Cook G. 2016. Oviposition preference and larval performance of PubMed
Rohde, K. , Dreier E., and Hochkirch A. 2015. Sex‐specific phenotypic plasticity in response to the trade‐off between developmental time and body size supports the dimorphic niche hypothesis. Biol. J. Linn. Soc. 115:48–57.
Sakashita, T. , Nakasuji F., and Fujisaki K. 1997. Effects of temperature and photoperiod on nymphal development of the stink bug,
Sarfraz, M. , Dosdall L. M., and Keddie B. A. 2007. Resistance of some cultivated Brassicaceae to infestations by PubMed
Sarfraz, M. , Dosdall L. M., and Keddie B. A. 2010. Performance of the specialist herbivore
Schoeller, E. N. , and Redak R. A. 2018. Temperature‐dependent development and survival of giant whitefly PubMed
Shimoji, Y. 2011. Effect of temperature on the development of the West Indian sweet potato weevil,
Singh, P. , van Bergen E., Brattström O., Osbaldeston D., Brakefield P. M., and Oostra V. 2020. Complex multi‑trait responses to multivariate environmental cues in a seasonal butterfly. Evol. Ecol. 34:713–734.
Sithole, R. , Löhr B., and Tagwireyi P. 2017. The influence of temperature on life history traits of
Skovgard, H. , and Nachman G. 2016. Temperature‐ and age‐dependent survival, development, and oviposition rates of the pupal parasitoid PubMed
Smith, A. M. 1984. Larval instar determination and temperature‐development studies of immature stages of the common armyworm,
Steigenga, M. J. , and Fischer K. 2009. Fitness consequences of variation in developmental temperature in a butterfly. Journal of Thermal Biology. 34:244–249.
Stenseng, L. , Skovgard H., and Holter P. 2003. Life table studies of the pupal parasitoid
Stevens, M. M. 1998. Development and survival of
Stoyenoff, J. L. , Witter J. A., Montgomery M. E., and Chilcote C. A. 1994. Effects of host switching on gypsy moth ( PubMed
Strom, B. L. , and Hain F. P. 1996. Host choice of late instar gypsy moths (Lepidoptera: Lymantriidae) between loblolly pine and sweetgum. Environ. Entomol. 25:603–610.
Syme, P. D. 1972. The influence of constant temperatures on the non‐diapause development of
Tang, J. ‐ J. , He H. ‐ M., Geng T., Fu S., and Xue F. ‐ S. 2016. Life history responses of the cabbage beetle
Terada, K. , Matsumura K., and Miyatake T. 2019. Effects of temperature during successive generations on life‑history traits in a seed beetle
Teulon, D. A. J. , and Penman D. R. 1991. Effects of temperature and diet on oviposition rate and development time of the New Zealand flower thrips,
Thiery, D. , and Moreau J. 2005. Relative performance of European grapevine moth ( PubMed
Thompson, L. M. , Faske T. M., Banahene N., Grim D., Agosta S. J., Parry D., et al. 2017. Variation in growth and developmental responses to supraoptimal temperatures near latitudinal range limits of gypsy moth
Tian, S. , Gu T., Chen C., Zhao X., Liu P., and Hao D. 2020. The effects of temperature and host size on the development of
Tochen, S. , Dalton D. T., Wiman N., Hamm C., Shearer P. W., and Walton V. M. 2014. Temperature‐related development and population parameters for PubMed
Togashi, K. , and Kodani J. 1990. Effect of temperature on the development of
Tokuda, M. , and Matsumura M. 2005. Effect of temperature on the development and reproduction of the maize orange leafhopper
Tomberlin, J. K. , Adler P. H., and Myers H. M. 2009. Development of the black soldier fly (Diptera: Stratiomyidae) in relation to temperature. Environ. Entomol. 38:930–934. PubMed
Toyoshima, S. , Arai T., and Yaginuma K. 2010. Effect of constant temperatures on the development of peach fruit moth,
Traore, L. , Pilon J. ‐ G., Fournier F., and Boivin G. 2006. Adaptation of the developmental process of
Tsukada, M. , Asai M., and Higuchi H. 2005. Developmental period and adult size of
Tsukada, M. , Tanaka D., and Higuchi H. 2008. Thermal requirement for development of
Ugine, T. A. , Sanderson J. P., and Wraight S. P. 2007. Developmental times and life tables for shore flies, PubMed
Ullah, M. S. , and Lim U. T. 2015. Life history characteristics of PubMed
Urbaneja, A. , Hinarejos R., Llacer E., Garrido A., and Jacas J. ‐ A. 2002. Effect of temperature on life history of PubMed
Uyi, O. O. , Zachariades C., Hill M. P., and McConnachie A. J. 2016. Temperature‐dependent performance and potential distribution of
Varikou, K. , Tsitsipis I., Alexandrakis V., and Hoddle M. 2009. Effect of temperature on the development and longevity of
Walker, P. W. 2011. Biology and development of
Wanderley, M. J. A. , and Ramalho F. S. 1999. Effects of the temperature on the development of
Wang, X. G. , and Messing R. H. 2004. Fitness consequences of body‐size‐dependent host species selection in a generalist ectoparasitoid. Biological Control. 31:227–236.
Wang, L. , Shi P., Chen C., and Xue F. 2013. Effect of temperature on the development of PubMed
Wang, X. ‐ G. , Serrato M. A., Son Y., Walton V. M., Hogg B. N., and Daane K. M. 2018. Thermal performance of two indigenous pupal parasitoids attacking the invasive PubMed
Weathersbee, A. A. , McKenzie C. L., and Tang Y. Q. 2004. Host plant and temperature effects on PubMed
Weaver, D. K. , and Throne J. E. 1994. Life history data for
Willott, S. J. , and Hassall M. 1998. Life‐history responses of British grasshoppers (Orthoptera: Acrididae) to temperature change. Funct. Ecol. 12:232–241.
Woodson, W. D. , and Jackson J. J. 1996. Developmental rate as a function of temperature in northern corn rootworm (Coleoptera: Chrysomelidae). Ann. Entomol. Soc. Am. 89:226–230.
Xia, Q. ‐ W. , Chen C., Tang J. ‐ J., He H. ‐ M., and Xue F. ‐ S. 2019. A reverse temperature‐size rule associated with a negative relationship between larval development time and pupal weight in a tropical population of
Xiao, L. , He H. ‐ M., Huang L. ‐ L., Geng T., Fu S., and Xue F. ‐ S. 2016. Variation of life‐history traits of the Asian corn borer, PubMed PMC
Yasuda, H. , and Dixon A. F. G. 2002. Sexual size dimorphism in the two spot ladybird beetle
Yi, S. ‐ J. , Hopkins R. J., Chen X. ‐ Y., Chen Z. ‐ M., Wang X., and Huang G. ‐ H. 2020. Effects of temperature on the development and fecundity of
Zamani, A. A. , Talebi A., Fathipour Y., and Baniameri V. 2007. Effect of temperature on life history of PubMed
Zerbino, M. S. , Altier N. A., and Panizzi A. R. 2013. Effect of photoperiod and temperature on nymphal development and adult reproduction of
Zhang, S. ‐ C. , Zhu F., Zheng X. ‐ L., Lei C. ‐ L., and Zhou X. ‐ M. 2012. Survival and developmental characteristics of the predatory bug
Altermatt, F. 2010. Climatic warming increases voltinism in European butterflies and moths. Proc. R. Soc. B Biol. Sci. 277:1281–1287. PubMed PMC
Angilletta, M. J. 2009. Thermal adaptation: a theoretical and empirical synthesis. Oxford Univ. Press, Oxford, U.K.
Angilletta, M. J. , and Dunham A. E.. 2003. The temperature‐size rule in ectotherms: simple evolutionary explanations may not be general. Am. Nat. 162:332–342. PubMed
Angilletta, M. J. , Niewiarowski P. H., and Navas C.. 2002. The evolution of thermal physiology in ectotherms. J. Therm. Biol. 27:249–268.
Angilletta, M. J. , Steury T. D., and Sears M. W.. 2004. Temperature, growth rate, and body size in ectotherms: fitting pieces of a life‐history puzzle. Integr. Comp. Biol. 44:498–509. PubMed
Arcus, V. L. , Prentice E. J., Hobbs J. K., Mulholland A. J., Van der Kamp M. W., Pudney C. R., et al. 2016. On the temperature dependence of enzyme‐catalyzed rates. Biochemistry. 55:1681–1688. PubMed
Atkinson, D. 1994. Temperature and organism size – a biological law for ectotherms? Adv. Ecol. Res. 25:1–58.
Back, J. A. , and King R. S. 2013. Sex and size matter: ontogenetic patterns of nutrient content of aquatic insects. Freshw. Sci. 32:837–848.
Badyaev, A. V. 2002. Growing apart: an ontogenetic perspective on the evolution of sexual size dimorphism. Trends Ecol. Evol. 17:369–378.
Bennett, J. M. , Sunday J., Calosi J., Villalobos F., Martinez B., Molina‐Venegas R., et al. 2021. The evolution of critical thermal limits of life on Earth. Nat. Commun. 12:1198. PubMed PMC
Blanckenhorn, W. U. 2000. The evolution of body size: what keeps organisms small? Q. Rev. Biol. 75:385–407. PubMed
Blanckenhorn, W. U. , Dixon A. F. G., Fairbairn D. J., Foellmer M. W., Gibert P., van der Linde K., et al. 2007. Proximate causes of Rensch's rule: does sexual size dimorphism in arthropods result from sex differences in development time? Am. Nat. 169:245–257. PubMed
Blanckenhorn, W. U. , Berger D., Rohner P. T., Schäfer M. A., Akashi H., and Walters R. J. 2021. Comprehensive thermal performance curves for yellow dung fly life history traits and the temperature‐size‐rule. J.ThermaBiology. 100:103069. PubMed
Bodensteiner, B. L. , Agudelo‐Cantero G. A., Arietta A. Z. A., Gunderson A. R., Muñoz M. M., Refsnider J. M., et al. 2020. Thermal adaptation revisited: how conserved are thermal traits of reptiles and amphibians? J. Exp. Zool. A. 335:173–194. PubMed
Breed, G. A. , Stichter S., and Crone E. E. 2013. Climate‐driven changes in northeastern US butterfly communities. Nat. Clim. Change. 3:142–145.
Catullo, R. A. , Llewelyn J., Phillips B. L., and Moritz C. C. 2019. The potential for rapid evolution under anthropogenic climate change. Curr. Biol. 29:R996–R1007. PubMed
Charnov, E. L. 1982. The theory of sex allocation. Princeton Univ. Press, Princeton, NJ. PubMed
Chazot, N. , Condamine F. L., Dudas G., Peña C., Kodandaramaiah U., Matos‐Maraví P., et al. 2021. Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush‐footed butterflies. Nat. Commun. 12:5717. PubMed PMC
Chelini, M. ‐ C. , Delong J. P., and Hebets E. A. 2019. Ecophysiological determinants of sexual size dimorphism: integrating growth trajectories, environmental conditions, and metabolic rates. Oecologia. 191:61–71. PubMed
Chown, S. L. , Hoffmann A. A., Kristensen T. N., Angilletta M. J., Stenseth N. C., and Pertoldi C. 2010. Adapting to climate change: a perspective from evolutionary physiology. Clim. Res. 43:3–15.
Cossins, A. R. , and Bowler K. 1987. Temperature biology of animals. Chapman and Hall, Lond.
Crowley, S. R. 1985. Thermal sensitivity of sprint‐running in the lizard PubMed
Davidowitz, G. , and Nijhout H. F. 2004. The physiological basis of reaction norms: the interaction among growth rate, the duration of growth and body size. Integr. Comp. Biol. 44:443–449. PubMed
Davidowitz, G. , D'Amico L. J., and Nijhout H. F. 2004. The effects of environmental variation on a mechanism that controls insect body size. Evol. Ecol. Res. 6:49–62.
Day, T. , and Rowe L. 2002. Developmental thresholds and the evolution of reaction norms for age and size at life‐history transitions. Am. Nat. 159:338–350. PubMed
Dmitriew, C. M. 2011. The evolution of growth trajectories: what limits growth rate? Biol. Rev. 86:97–116. PubMed
Fairbairn, D. J. 1997. Allometry for sexual size dimorphism: pattern and process in the coevolution of body size in males and females. Annu. Rev. Ecol. Syst. 28:659–687.
Fischer, K. , and Fiedler K. 2002. Life‐history plasticity in the butterfly
Fischer, K. , Kölzow N., Höltje H., and Karl I. 2011. Assay conditions in laboratory experiments: is the use of rather than fluctuating temperatures justified when investigating temperature‐induced plasticity? Oecologia. 166:23–33. PubMed
Forster, J. , Hirst A. G., and Woodward G. 2011. Growth and development rates have different thermal responses. Am. Nat. 178:668–678. PubMed
Forster, J. , and Hirst A. G. 2012. The temperature‐size rule emerges from ontogenetic differences between growth and development rates. Funct. Ecol. 26:483–492.
Forster, J. , Hirst A. G., and Atkinson D. 2012. Warming‐induced reductions in body size are greater in aquatic than terrestrial species. Proc. Natl. Acad. Sci USA, 109:19310–19314. PubMed PMC
Ghalambor, C. K. , McKay J. K., Carroll S. P., and Reznick D. N. 2007. Adaptive versus non‐adaptive phenotypic plasticity and the potential for contemporary adaptation in new environments. Funct. Ecol. 21:394–407.
Ghosh, S. M. , Testa N. D., and Shingleton A. W. 2013. Temperature‐size rule is mediated by thermal plasticity of critical size in PubMed PMC
Gotthard, K. , and Nylin S. 1995. Adaptive plasticity and plasticity as an adaptation: a selective review of plasticity in animal morphology and life‐history. Oikos. 74:3–17.
Hertz, P. E. , Huey R. B., and Nevo E. 1983. Homage to Santa Anita: thermal sensitivity of sprint speed in agamid lizards. Evolution; Internation Journal of Organic Evolution. 37:1075–1084. PubMed
Hirst, A. G. , Horne C. R., and Atkinson D. 2015. Equal temperature‐size responses of the sexes are widespread within arthropod species. Proc. R. Soc. B Biol. Sci. 282:20152475. PubMed PMC
Hochachka, P. W. , and Somero G. N. 2002. Biochemical adaptation: mechanism and process in physiological evolution. Oxford Univ. Press, Oxford, U.K.
Hoffmann, A. A. , and Sgro C. M. 2011. Climate change and evolutionary adaptation. Nature. 470:479–485. PubMed
Hoffmann, A. A. , Chown S. L., and Clusella‐Trullas S. 2013. Upper thermal limits in terrestrial ectotherms: how constrained are they? Funct. Ecol. 27:934–949.
Honek, A. 1993. Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos. 66:483–492.
Horne, C. R. , Hirst A. G., and Atkinson D. 2015. Temperature‐size responses match latitudinal‐size clines in arthropods, revealing critical differences between aquatic and terrestrial species. Ecol. Lett. 18:327–335. PubMed
Horne, C. R. , Hirst A. G., and Atkinson D. 2017. Seasonal body size reductions with warming covary with major body size gradients in arthropod species. Proc. R. Soc. B Biol. Sci. 284:20170238. PubMed PMC
James, F. C. 1970. Geographic size variation in birds and its relationship to climate. Ecology. 51:365–390.
Jarosik, V. , Honek A., Magarey R. D., and Skuhrovec J. 2011. Developmental database for phenology models: related insect and mite species have similar thermal requirements. J. Econ. Entomol. 104:1870–1876. PubMed
Kause, A. , Saloniemi I., Haukioja E., and Hanhimäki S. 1999. How to become large quickly: quantitative genetics of growth and foraging in a flush feeding lepidopteran larva. J. Evol. Biol. 12:471–482.
Kingsolver, J. G. , Massie K. R., Ragland G. J., and Smith M. H. 2007. Rapid population divergence in thermal reaction norms for an invading species: breaking the temperature–size rule. J. Evol. Biol. 20:892–900. PubMed
Kingsolver, J. G. , and Huey R. B. 2008. Size, temperature, and fitness: three rules. Evol. Ecol. Res. 10:251–268.
Klepsatel, P. , Gáliková M., De Maio N., Huber C. D., Schlötterer C., and Flatt T. 2013. Variation in thermal performance and reaction norms among populations of PubMed
Koricheva, J. , Gurevitch J., and Mengersen K., eds. 2013. Handbook of meta‐analysis in ecology and evolution. Princeton Univ. Press, Princeton, NJ.
Kulma, M. , Kourimská L., Plachý V., Božik M., Adámková A., and Vrabec V. 2019. Effect of sex on the nutritional value of house cricket, Acheta domestica L. Food Chem, 272:267–272. PubMed
Kutcherov, D. 2016. Thermal reaction norms can surmount evolutionary constraints: comparative evidence across leaf beetle species. Ecol. Evol. 6:4670–4683. PubMed PMC
Lailvaux, S. P. 2007. Interactive effects of sex and temperature on locomotion in reptiles. Integr. Comp. Biol. 47:189–199. PubMed
Logan, M. L. , Minnaar I. A., Keegan K. M., and Clusella‐Trullas S. 2020. The evolutionary potential of an insect invader under climate change. Evolution; Internation Journal of Organic Evolution. 74:132–144. PubMed
Lovich, J. E. , and Gibbons J. W. 1992. A review of techniques for quantifying sexual size dimorphism. Growth, Development, and Aging. 56:269–281. PubMed
Marshall, K. E. , Gotthard K., and Williams C. M. 2020. Evolutionary impacts of winter climate change on insects. Curr. Opin. Insect Sci. 41:54–62. PubMed
Meister, H. , Hämäläinen H. R., Valdma D., Martverk M., and Tammaru T. 2018. How to become larger: ontogenetic basis of among‐population size differences in a moth. Entomol. Exp. Appl. 166:4–16.
Michonneau, F. , Brown J. W., and Winter D. J. 2016. rotl: an R package to interact with the Open Tree of Life data. Methods Ecol. Evol. 7:1476–1481.
Moghadam, N. N. , Sidhu K., Summanen P. A. M., Ketola T., and Kronholm I. 2020. Quantitative genetics of temperature performance curves of PubMed
Molleman, F. , Javoiš J., Esperk T., Teder T., Davis R. B., and Tammaru T. 2011. Sexual differences in weight loss upon eclosion are related to life history strategy in Lepidoptera. J. Insect Physiol. 57:712–722. PubMed
Nakagawa, S. , Noble D. W. A., Senior A. M., and Lagisz M. 2017. Meta‐evaluation of meta‐analysis: ten appraisal questions for biologists. BMC Biology. 15:18. PubMed PMC
OpenTree , Cranston, K. A. , Redelings B., Sanchez Reyes L. L., Allman J., McTavish E. J., et al. 2022. Open tree of life taxonomy. Version 3.3. Zenodo. 10.5281/zenodo.3937750. DOI
Parmesan, C. 2006. Ecological and evolutionary responses to recent climate change. Annu. Rev. Ecol. Syst. 37:637–669.
Parmesan, C. , Ryrholm N., Stefanescu C., Hill J. K., Thomas C. D., Descimon H., et al. 1999. Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature. 399:579–583.
Pigliucci, M. 2001. Phenotypic plasticity: beyond nature and nurture. Johns Hopkins Univ. Press, Baltimore, MD.
Pottier, P. , Burke S., Drobniak S. M., Lagisz M., and Nakagawa S. 2021. Sexual (in)equality? A meta‐analysis of sex differences in thermal acclimation capacity across ectotherms. Funct. Ecol. 35:2663–2678.
R Core Team 2020. R: a language and environment for statistical computing. Version 3.6.3. R Foundation for Statistical Computing, Vienna.
Ratte, H. T. 1984. Temperature and insect development. Pp 33–66
Rohner, P. T. , and Blanckenhorn W. U. 2018. A comparative study of the role of sex‐specific condition dependence in the evolution of sexually dimorphic traits. Am. Nat. 192:E202–E215. PubMed
Rohner, P. T. , Teder T., Esperk T., Lüpold S., and Blanckenhorn W. 2018. The evolution of male‐biased sexual size dimorphism is associated with increased body size plasticity in males. Funct. Ecol. 32:581–591.
Seebacher, F. , White C. R., and Franklin C. E. 2015. Physiological plasticity increases resilience of ectothermic animals to climate change. Nat. Clim. Change. 5:61–66.
Sgro, C. M. , Terblanche J. S., and Hoffmann A. A. 2016. What can plasticity contribute to insect responses to climate change? Annu. Rev. Entomol. 61:433–451. PubMed
Stearns, S. C. 1992. The evolution of life histories. Oxford Univ. Press, Lond.
Stillwell, R. C. , and Fox C. W. 2007. Environmental effects on sexual size dimorphism of a seed‐feeding beetle. Oecologia. 153:273–280. PubMed
Stillwell, R. C. , and Davidowitz G. 2010. Sex differences in phenotypic plasticity of a mechanism that controls body size: implications for sexual size dimorphism. Proc. R. Soc. B Biol. Sci. 277:3819–3826. PubMed PMC
Stillwell, R. C. , Blanckenhorn W. U., Teder T., Davidowitz G., and Fox C. W. 2010. Sex differences in phenotypic plasticity affect variation in sexual size dimorphism in insects: from physiology to evolution. Annu. Rev. Entomol. 55:227–245. PubMed PMC
Svensson, E. I. , Gomez‐Llano M., and Waller J. T. 2020. Selection on phenotypic plasticity favors thermal canalization. Proc. Natl. Acad. Sci. USA. 117:29767–29774. PubMed PMC
Tammaru, T. , Esperk T., and Castellanos I. 2002. No evidence for costs of being large in females of PubMed
Tammaru, T. , Nylin S., Ruohomäki K., and Gotthard K. 2004. Compensatory responses in lepidopteran larvae: a test of growth rate maximisation. Oikos. 107:352–362.
Tammaru, T. , Esperk T., Ivanov V., and Teder T. 2010. Proximate sources of sexual size dimorphism in insects: locating constraints on larval growth schedules. Evol. Ecol. 24:161–175.
Teder, T. 2014. Sexual size dimorphism requires a corresponding sex difference in development time: a meta‐analysis in insects. Funct. Ecol. 28:479–486.
Teder, T. 2020. Phenological responses to climate warming in temperate moths and butterflies: species traits predict future changes in voltinism. Oikos. 129:1051–1060.
Teder, T. , and Tammaru T. 2005. Sexual size dimorphism within species increases with body size in insects. Oikos. 108:321–334.
Teder, T. , Tammaru T., and Esperk T. 2008. Dependence of phenotypic variance in body size on environmental quality. Am. Nat. 172:223–232. PubMed
Teder, T. , Vellau H., and Tammaru T. 2014. Age and size at maturity: a quantitative review of diet‐induced reaction norms in insects. Evolution; Internation Journal of Organic Evolution. 68:3217–3228. PubMed
Teder, T. , Kaasik A., Taits K., and Tammaru T. 2021. Why do males emerge before females? Sexual size dimorphism drives sexual bimaturism in insects. Biol. Rev. 96:2461–2475. PubMed
Thornhill, R. , and Alcock J. 1983. The evolution of insect mating systems. Harvard Univ. Press, Cambridge, MA.
Tiitsaar, A. , Valdma D., Õunap E., Remm J., Teder T., and Tammaru T. 2019. Distribution of butterflies (Lepidoptera: Papilionoidea) in Estonia: results of a systematic mapping project reveal long‐term trends. Ann. Zool. Fenn. 56:147–185.
van Damme, R. , Bauwens D., and Verheyen R. F. 1990. Evolutionary rigidity of thermal physiology: the case of the cool temperate lizard
van der Have, T. M. , and Jong G. 1996. Adult size in ectotherms: temperature effects on growth and differentiation. J. Theor. Biol. 183:329–340.
Verberk, W. C. E. P. , Atkinson D., Hoefnagel K. N., Hirst A. G., Horne C. R., and Siepel H. 2021. Shrinking body sizes in response to warming: explanations for the temperature size–rule with special emphasis on the role of oxygen. Biol. Rev. 96:247–268. PubMed PMC
Viechtbauer, W. 2010. Conducting meta‐analyses in R with the metafor package. J. Stat. Softw. 36:1–48.
Weaving, H. , Terblanche J. S., Pottier P., and English S. 2022. Meta‐analysis reveals weak but pervasive plasticity in insect thermal limits. Nat. Commun. 13:5292. PubMed PMC
Wiklund, C. , and Fagerström T. 1977. Why do males emerge before females? A hypothesis to explain the incidence of protandry in butterflies. Oecologia. 31:153–158. PubMed
Zeuss, D. , Brunzel S., and Brandl R. 2017. Environmental drivers of voltinism and body size in insect assemblages across. Europe. Global Ecol. Biogeogr. 26:154–165.
Zuo, W. , Moses M. E., West G. B., Hou C., and Brown J. H. 2012. A general model for effects of temperature on ectotherm ontogenetic growth and development. Proc. R. Soc. B Biol. Sci. 279:1840–1846. PubMed PMC
Dryad
10.5061/dryad.djh9w0w3q