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Complex Patterns of Phenotypic Plasticity: Interactive Effects of Temperature During Rearing and Oviposition

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Complex Patterns of Phenotypic Plasticity: Interactive Effects of Temperature During Rearing and Oviposition Ecology, 86(4), 2005, pp. 924±934 q 2005 by the Ecological Society of America COMPLEX PATTERNS OF PHENOTYPIC PLASTICITY: INTERACTIVE EFFECTS OF TEMPERATURE DURING REARING AND OVIPOSITION R. CRAIG STILLWELL1 AND CHARLES W. F OX Department of Entomology, University of Kentucky, S-225 Ag Science Center North, Lexington, Kentucky 40546-0091 USA Abstract. Temperature profoundly affects growth and life history traits in ectothermic animals through selection (i.e., genetic) and through direct effects on the phenotype (i.e., nongenetic/plasticity). We examined the effects of rearing temperature (248,308, and 368C) on adult body size and development time and the interactive effects of temperature ex- perienced during rearing and oviposition on several life history traits (age-at-®rst-repro- duction, fecundity, egg size, egg development, and egg hatching) in two populations of the seed beetle, Stator limbatus, collected at different elevations. The higher elevation popu- lation was larger and matured sooner than the low-elevation population when raised at the lower temperature, but the reverse was true at the higher temperature suggesting that these populations have adapted to local temperature. There were interactions between the effects of rearing temperature and oviposition temperature for age-at-®rst-reproduction, fecundity, egg development, egg hatching, and two composite measures of ®tness, generating complex reaction norms. The most dramatic example of this was a large maternal effect on egg hatching; females raised at low temperature produced eggs that had substantially reduced hatching when laid at high temperature. Our experimental design also allowed us to explore the adaptive signi®cance of acclimation. Beetles reared at intermediate or low temperature had the highest ®tness at multiple oviposition temperatures. There was little support for the ``bene®cial acclimation hypothesis,'' which predicts that beetles should have higher ®tness at the temperature at which they were reared; acclimation had only a small effect on ®tness. This study shows that temperature-mediated plasticity can be complex, but these complex patterns can yield new insights into the evolution of phenotypic plasticity. Key words: acclimation; adaptation; bene®cial acclimation hypothesis; body size; maternal ef- fects; phenotypic plasticity; Stator limbatus; temperature. INTRODUCTION in nature. Body size and egg size of ectotherms exhibit clinal variation along latitudinal (e.g., Lonsdale and For many ectothermic animals, the temperature ex- Levinton 1985, Armbruster et al. 2001) and altitudinal perienced during development strongly affects many gradients (e.g., Berven 1982). When individuals are growth and life history traits. For instance, body size reared in a common environment, these differences are (Atkinson 1994), development time (Atkinson 1994), usually found to be partially genetically based. In Dro- and egg/offspring size (Fox and Czesak 2000) generally sophila melanogaster, body size clines are often re- increase with decreasing temperature, whereas fecun- peatable across continents (e.g., James et al. 1995, dity (e.g., Fischer et al. 2003a) generally declines with Van't Land et al. 1995). These clines can evolve rap- decreasing temperature. These phenotypic responses idly, only a couple of decades after introduction to a may be a result of adaptation to different thermal en- new continent (Huey et al. 2000), indicating strong vironments or may be an unavoidable consequence of natural selection on either body size, egg size, or some a temperature effect on the organism's physiology dur- correlated trait. Laboratory natural selection experi- ing development (developmental plasticity). The extent to which temperature-mediated natural selection vs. the ments, in which insects are allowed to adapt to high environmental effect of temperature differentially af- or low temperature, also demonstrate that both body fect traits at different temperatures has generated de- size and egg size evolve to be larger at colder tem- bate between adaptive (genetic) and developmental peratures (Partridge et al. 1994, Azevedo et al. 1996; (nongenetic) hypotheses (Van Voorhies 1996, 1997, but see Santos et al. 2004). Mousseau 1997, Partridge and Coyne 1997). Nongenetic responses to developmental temperature Evidence for genetic adaptation to temperature (phenotypic plasticity) are widespread. For example, comes from studies of patterns of geographic variation growth at lower temperature results in increased adult body size in .80% of ectothermic animals (Atkinson 1994), and many arthropods typically lay larger eggs Manuscript received 22 March 2004; accepted 26 July 2004; ®nal version received 21 September 2004. Corresponding Editor: at lower temperatures (Fox and Czesak 2000). Non- E. Brodie III. genetic responses to developmental temperature are 1 E-mail: [email protected] thus very similar to those produced by evolution at 924 April 2005 COMPLEX PATTERNS OF PLASTICITY 925 different temperatures making it dif®cult to distinguish and the interactive effects of rearing vs. oviposition between genetic (evolution due to selection) and non- temperature and to assess the adaptive signi®cance of genetic (plasticity) causes for geographic patterns. acclimation. Within central Arizona, USA, S. limbatus Common garden and reciprocal transplant experiments experiences large daily (ranging from 248 to 398C; are required to disentangle these factors. mean minimum daily temperature compared to mean Adding to this complexity, patterns of phenotypic maximum daily temperature in Phoenix, Arizona) and plasticity may change if the temperature encountered spatial (258±318C; monthly mean in Oracle, Arizona, in an earlier vs. a later life stage interact to affect a compared to Phoenix, Arizona; Western Regional Cli- phenotype. For instance, immature stages of many in- mate Center, Desert Research Institute) variation in sects develop at different times of the year and in other temperature during August when beetles are most ac- physical localities than adults, subjecting these life tive. S. limbatus is a generalist seed parasite of le- stages to different thermal environments. Also, im- gumes; adults are the only dispersing stage of the life matures are less mobile than adults and are often unable cycle, with larvae being restricted to the seed their to leave unfavorable thermal environments. Neverthe- mother has chosen for them. Since larvae cannot move less, few studies have considered both the separate and between seeds they cannot move between thermal en- interactive effects of temperature experienced during vironments. immature development (rearing) vs. adult (oviposition) In this study, we examine two populations of S. lim- stages of the life cycle (Fox and Czesak 2000). We batus from central Arizona that occur at different el- need to understand how these interactions affect re- evations (Phoenix, ;500 m above sea level; Oracle, action norm shape to predict response to selection in ;1400 m above sea level) and experience different more complex environments. local thermal environments (mean temperature differ- Studies on the effects of temperature experienced at ence in August of ;68C). Our a priori expectations an early and later life stage provide a unique oppor- were that these populations are adapted to a ``warm'' tunity to study the adaptive signi®cance of acclimation and ``cool'' environment and should be genetically dif- (a nongenetic, physiological alteration in a phenotype ferentiated in a number of traits. We ®rst assessed how caused by a change in the environment). It is commonly temperature during rearing affects adult body size and assumed that development at a certain temperature will larval development time in both populations. We then enhance ®tness in the adult stage at that temperature examined the separate and interactive effects of tem- (``bene®cial acclimation hypothesis''; Leroi et al. perature experienced by beetles during rearing vs. ovi- 1994). Alternatively, acclimation may be nonadaptive position periods of the life cycle on age-at-®rst-repro- if rearing in one environment enhances ®tness in al- duction, fecundity, egg size, egg development, and egg ternate environments to which the organism is not ac- hatching. Finally, using the approach described by climated (Huey et al. 1999). For example, development Huey et al. (1999) we tested the bene®cial acclimation, at an intermediate (``optimal developmental tempera- optimal developmental temperature, hotter is better, ture hypothesis''), low (``colder is better hypothesis''), and colder is better hypotheses. or high (``hotter is better hypothesis'') temperature may enhance ®tness in a variety of adult thermal environ- METHODS ments. Recently, factorial designs have been developed Natural history of Stator limbatus to explore the adaptive signi®cance of acclimation (Huey and Berrigan 1996). These designs and recently The seed beetle, Stator limbatus (Horn) (Coleoptera: developed statistical models allow for several com- Chrysomelidae: Bruchinae), is distributed from north- peting hypotheses to be tested simultaneously (Huey ern South America to the southwestern United States et al. 1999). Assessments using this approach have (Johnson and Kingsolver 1976, Johnson et al. 1989, shown that while the bene®cial acclimation hypothesis Nilsson and Johnson 1993). It is a generalist seed her- is supported in some cases, alternative hypotheses often bivore that has been collected from .70 species of have a greater in¯uence
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