Is bigger really bigger? Differential responses to temperature in measures of body size of the mosquito, Aedes albopictus

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Abstract

When confronted with variation in temperature, most ectotherms conform to a growth rule that “hotter is smaller”. This phenomenon can have important implications on population dynamics, interactions with other species, and adaptation to new environments for arthropods. However, the impact of other environmental factors and genetics may affect that general rule. Furthermore, most studies measure a single body part, and do not examine how temperature and other factors alter the allometric relationship between measurements of growth. In this study, we test the hypothesis that temperature and nutrition, while strongly affecting growth, do not change the allometric relationship between body mass and wing length in the mosquito Aedes albopictus. We tested this hypothesis by growing larval mosquitoes from two populations at five temperatures with three food levels. Contrary to our hypothesis, we find that temperature has a profound effect on allometry, with higher temperatures resulting in mosquitoes with shorter wings and greater body mass, and that the effects of temperature are dependent upon available food and population origin. We therefore reject our hypothesis and propose several testable mechanisms that will provide greater insight into the relationship between temperature, food, and measures of growth.

Highlights

► We propose a hypothesis of allometry across temperature and nutrients. ► The allometric relationship between wing length and mass depends on temperature. ► Cooler conditions resulted in longer wings per body mass. ► Warmer conditions results in shorter wings per body mass. ► The adaptive significance of our finding awaits further experimentation.

Introduction

The response of ectotherms, particular invertebrates, to variation in temperature during growth phases has generally been summarized as the temperature size rule, in which “hotter is smaller”, such that ectotherms exposed to warmer temperatures achieve a smaller adult size (Atkinson, 1994, Kingsolver and Huey, 2008). Indeed there is tremendous empirical support for this “rule”, with over 80% of studies supporting this finding, the majority of which are from insects in both terrestrial and aquatic habitats (Atkinson, 1994, Atkinson, 1995). Exceptions to this rule are also often insects from a diverse set of orders, including Diptera, Ornithoptera, Lepidoptera and most especially, Ephemeroptera (Atkinson, 1994, Atkinson, 1995). Adherence to this rule, or the degree of adherence, is plastic within a species, reflecting local adaptation of thermal reaction norms (Gilchrist and Huey, 2004) and the effects of other ecological conditions, such as diet and nutrition (Diamond and Kingsolver, 2010).

Most studies of the effects of temperature on adult size in ectotherms use a single measurement of growth (Atkinson, 1994). A major assumption of many studies comparing final size of adult holometabolous insects is a tight allometric correlation between the measured body part (e.g., wing length, thorax width, etc.) and other measurements of size (e.g., other body parts, dry weight, total length, etc.) for each individual. The physiological mechanisms for this correlation are not well understood, and may include metabolic rate forcing, changes in the timing of hormone release, sensitivity of target tissues, or some combination of these mechanisms (Nijhout, 2003, Nijhout and Grunert, 2010, Nijhout et al., 2010). However, these physiological mechanisms of enforcing allometry may be sensitive to type of environmental variation, such as temperature or nutrition, which may change the allometric relationships between body parts (Diamond and Kingsolver, 2010, Shingleton et al., 2007). Consequently, any temperature-size rule may depend upon what growth measurement is being used and there may be differences in the temperature-size rule depending upon nutrition (Diamond and Kingsolver, 2010).

Many studies of mosquito growth use a single measurement of body size (often wing length) to compare individual growth or estimate population growth, based upon the assumption that this body part correlates with other aspects of mosquito bodies that determine fitness (Hawley, 1985, Juliano, 1998, Livdahl and Sugihara, 1984, Lounibos et al., 1993). This is based on correlation studies comparing measurements of body size or wing length with weight and weight with fecundity in container inhabiting Aedes mosquitoes (Armbruster and Hutchinson, 2002, Blackmore and Lord, 2000, Briegel and Timmermann, 2001, Koenraadt, 2008, Leisnham et al., 2009, Nasci, 1990). These studies find a high degree of correlation between weight and wing length across many species, with explained variance ranging from 59% to 92%, and considerably less explained variation between measurement of body size and fecundity (r2 between 0.12 and 0.83). However, most of these studies generated diversity in sizes by varying food or initial larval density and none examined the effects of temperature on these allometries or on fecundity. As in other ectotherms, increased temperature has generally been associated with shorter development time and smaller adults in a wide array of mosquito species (Briegel and Timmermann, 2001, Brust, 1967, Lyimo et al., 1992, Ragland and Kingsolver, 2008, Rueda et al., 1990, Van den Heuvel, 1963, Westbrook et al., 2010). However, there have been some notable exceptions to the hotter is smaller rule for mosquitoes. Lounibos et al. (2002) found a significant increase in male dry mass in adult Aedes albopictus reared at 30 °C relative to those reared at 24 °C and a non-significant increase in female dry mass. Wing length data were not reported. Additionally, in one of the few studies that report both weight and wing length, Nayar (1969) found an increase in dry weight at intermediate temperatures (a “hump-shaped” relationship) while wing length decreased linearly at increasing temperatures in Aedes taeniorhynchus. In Anopheles there have been a couple of studies examining how temperature affects wing length and weight, both of which hint at a change in allometry across temperatures, although do not directly analyze an allometric variable (Koella and Lyimo, 1996, Lanciani and Le, 1995).

We tested the hypothesis that two measurements of total growth, wing length and adult dry weight of A. albopictus vary in the same manner in response to variation in larval temperature and nutrition, such that the allometry is insensitive to changes in environmental conditions. To avoid confounding effects of competition, we reared each mosquito individually. To determine whether these responses were conserved across different genotypes, we examined two populations of A. albopictus collected from widely separated areas in North America.

Section snippets

Mosquitoes

Mosquitoes used in this experiment were F1 mosquitoes from Tulsa, OK, collected from eggs in the summer of 2009 and F4 mosquitoes from an original population of A. albopictus eggs collected in the summer of 2008 in Palm Beach County, FL. The original collection of Florida mosquitoes included over 1500 eggs collected from 30 sites in urban Palm Beach County. Florida mosquitoes were maintained through three generations in the following conditions: 100 larvae/l of water infused with 4 g of live oak

Mortality

No mosquitoes survived to pupation in the 8.6 °C treatment. At 19.5, 23.6 and 27.4 °C there was high survival, with little variation by population or food regime (survival to adulthood across both populations and all food regimes: 87.5%; data available in supplementary data). However, at 14.3 °C there was lower survival than at higher temperatures (Table 1; survival to adulthood across both populations and all food regimes: 45.83%). This lower survival was similar across the two populations, and

Discussion

We found strong evidence that our two measures of body size, wing length and dry weight do not vary in the same direction with respect to different temperatures and food levels. Food level generally increased both wing length and weight, as has been noted in numerous other studies (Briegel and Timmermann, 2001, Juliano, 2009). However, the allometric relationship between wing length and weight showed significant variation as a function of food level, with smaller wings relative to mass at lower

Conclusions

We found a break in allometry between wing length and dry mass as function of temperature across different food regimes in two populations of A. albopictus. Specifically, mosquitoes were relatively heavier for their wing lengths at higher temperatures compared to lower temperatures, suggesting a plastic reaction norm to temperature, conserved over some environmental (food) and genetic variation (population origin). Our results suggest several proximate and ultimate questions for future

Acknowledgements

The authors wish to thank Talan Klein for helping measure wings and Greg Ragland, Harish Padmanabha, George Opit and Jack Dillwith for reading earlier versions of this manuscript. This work was supported by a grant from the Oklahoma Center for the Advancement of Science and Technology (OCAST HR09-157), by the Oklahoma Agricultural Experiment Station (OAES: Hatch Project 2702), and by the Multistate Hatch Project NE 1034Mosquitoes and Public Health” (MSS Project 2712).

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