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. Author manuscript; available in PMC: 2011 Oct 1.
Published in final edited form as: Biol J Linn Soc Lond. 2010 Oct 1;101(2):345–350. doi: 10.1111/j.1095-8312.2010.01497.x

Lifespan of a Ceratitis fruit fly increases with higher altitude

Pierre-François Duyck 1,2, Nikos A Kouloussis 3, Nikos T Papadopoulos 4, Serge Quilici 2, Jane-Ling Wang 5, Ci-Ren Jiang 6, Hans-Georg Müller 5, James R Carey 7
PMCID: PMC2971552  NIHMSID: NIHMS206777  PMID: 21057666

Abstract

Variation in lifespan may be linked to geographic factors. While latitudinal variation in lifespan has been studied for a number of species, altitude variation has received much less attention, particularly in insects. We measured the lifespan of different populations of the Natal fruit fly Ceratitis rosa along an altitudinal cline. For the different populations we first measured the residual longevity of wild flies by captive cohort approach and compared F1 generation from the same populations. We showed an increase in lifespan with higher altitude for a part of our data. For the field collected flies (F0) the average remaining lifespan increased monotonically with altitude for males but not for females. For the F1 generation, longevity of both males and females of the highest-altitude population was longer than for the two other lower-altitude populations. This relationship between altitude and lifespan may be explained by the effects of temperature on reproduction. Reproductive schedules in insects are linked to temperature: lower temperature, characteristic of high-altitude sites, generally slows down reproduction. Because of a strong trade-off between reproduction and longevity, we therefore observed a longer lifespan for the high- altitude populations. Other hypotheses such as different predation rates in the different sites are also discussed.

Keywords: Altitude, Biodemographic studies, Ceratitis rosa, Natal fruit fly, Longevity, Tephritidae

INTRODUCTION

Variation in longevity in the wild may be caused by different external factors. Classical theories on the evolution of senescence predict that populations that have experienced external high mortality rates will senesce more quickly (Williams et al., 2006). For example populations that have been subjected to high predation rate have evolved to a shorter lifespan (Reznick, Bryant & Holmes, 2006).

Variation in longevity may also be linked to geographic abiotic factors. Longevity in the wild may vary with latitude and altitude, in relation to temperature. Most studies on the relationship between senescence and geographic variation have been carried out on birds. Different studies showed that the senescence rate among bird species increases with latitude, as expected because of slow life-histories at low latitudes (Fogden, 1972; Møller, 2007; Wiersma et al., 2007). The shorter lifespan in birds from temperate compared to tropical climates may be explained by the fact that they have evolved in high basal metabolic rate linked to high thermogenic capacity (Wiersma et al., 2007). However in ectotherms, such as insects, lifespan usually increases with latitude and this variation of lifespan within species has been recently explained by the metabolic theory of ecology (Munch & Salinas, 2009).

While latitudinal variation in lifespan has been studied for a number of species, variation with altitude, in particular in insects, has received much less attention; probably because altitudinal clines involve shorter distances with gene flow between populations likely being important (Karl, Janowitz & Fischer, 2008). In a study on grasshoppers in California, Tatar et al. (1997) showed a decrease in longevity with high altitude. It was hypothesized that high elevation populations have evolved an accelerated senescence as a result of selection on reproductive schedules, which are potentially structured by severe winter conditions at the elevated sites. However reproductive schedules in insects are linked to temperature and lower temperature at high elevation sites should slow down reproduction. Experimentally increased reproductive activity is generally associated with decreased lifespan (Chapman et al., 1998; Gustafsson & Part, 1990; Williams, 1966). Because of this strong trade-off between reproduction and longevity, longer lifespan should be observed in high elevation places. In a site where winter conditions are not strong enough to stop reproduction, we therefore predict an increase in lifespan with higher altitude.

We tested this prediction along an altitudinal gradient in a tropical area (La Réunion, an island in the South-Western Indian Ocean) using a Ceratitis fruit fly species. Ceratitis rosa is very closely genetically and ecologically related to the medfly C. capitata (Baliraine et al., 2004; De Meyer et al., 2008; Malacrida et al., 1996; Torti et al., 1998), which is an important model species for aging studies (Carey, 2001). Ceratitis rosa is present in Eastern and Southern Africa as well as in some Indian ocean islands (De Meyer et al., 2008). It invaded La Réunion in the mid-20th century and is now present in most parts of the island (Duyck, David & Quilici, 2006). Ceratitis rosa is able to develop on a wide range of temperatures and is therefore found from sea level up to an altitude of 1500 m. Pupae of this species survive better in humid compared to dry conditions (Duyck et al., 2006). As for other fruit fly species, development and reproductive ability of C. rosa are linked to temperature with lower temperature causing decreasing ovarian maturation rates and therefore decreasing fecundity (Duyck & Quilici, 2002).

The objective of the present study was to test the prediction that the lifespan of C. rosa increases with altitude. We measured the lifespan of different populations of C. rosa along an altitudinal cline. For the different populations we first measured the residual longevity of wild flies by the captive cohort approach (Carey et al., 2008). As differences in residual longevity may imply different longevities, different age structure or both, we measured lifespan and compared F1 generation from the same populations.

MATERIALS AND METHODS

Collection sites

We collected males and females of C. rosa from three sites along a transect of altitude (300, 600, 900 m) in La Réunion island (Indian Ocean, 21°20’S, 55°15’E) in December 2007 (Table 1). Each collection site consisted of a Creole garden with many fruit species and no insecticide applications. The seasonal characteristics of the sites vary systematically from low to high elevation with decreasing temperature and increasing rainfall with increasing altitude (Table 1).

Table 1.

Climatic parameters at the three study sites

Altitude (m)
300 600 900
Mean annual temperature (°C) 21.9 19.5 18.0
Minimum temperature (°C) 11.2 8.7 6.2
Maximum temperature (°C) 33.4 31.5 29.6
Mean annual rainfall (mm) 1100 1400 1700
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Lifespan measurement

In each site males and females fruit flies were collected for one day using 20 “Tephri-traps” (Sorygar, Madrid, Spain) with “3-lures” (Suterra, Chicago, USA), a nitrogen food based attractant for both sexes of various Ceratitis spp., but more effective for females than males (Epsky et al., 1999). These live-caught flies were then transported to the laboratory. For each site 92 flies (46 males and 46 females) were placed in individual containers for mortality measurement while remaining flies (100 to 200) were placed together in a cage (30 × 30 × 30 cm) in order to construct the F1 cohort. In each cage, an egg laying device with spaced holes containing a piece of Citrus was used to collect eggs. Larvae were reared on an artificial diet (Duyck & Quilici, 2002). After adult emergence from pupae, 92 flies (46 males and 46 females) were placed in individual cages for mortality measurement. In total (F0+F1) 552 flies were observed individually.

The experimental procedure followed standard material and methods for the study of Tephtitidae longevity (Carey, 2003). The study was conducted in the laboratory at 25 ± 1°C, 65 ± 10% R.H and 12:12 hour photoperiod. Light was provided by daylight tubes. Individual cages consisted of a transparent plastic cup, 12-cm high, 5-cm base diameter and 7.5-cm top diameter which was placed upside down, and glued to the lid of a plastic Petri dish (9-cm diameter) with adult food (a mixture of yeast hydrolyzate (ICN Biochemical, Aurora, USA) and sugar, 1:4), and water. Adult food was supplied ad libitum on the floor of the cage, and water was provided by a cotton wick that passed through a small hole in the Petri dish lid to an underlying Petri dish base, which was filled with water. A lateral window covered with mesh was perforated on the cup’s side for ventilation. Mortality in each individual cage was recorded daily.

Calculations and statistical analyses

Life expectancy at birth was calculated as ∑x=0∞1lx where lx is the fraction of the cohort alive at age × (Carey, 2001). Confidence intervals for life expectancy were estimated as the 2.5 and 97.5 percentiles of a bootstrap distribution resampled 1000 times (Caswell, 2001; Efron & Tibshirani, 1993).

After verification of normality, data longevities of F0 and F1 generation were subjected to a two-way analysis of variance (ANOVA) that included the effects of the sex (males, females), altitude (300, 600, 900 m), and interactions between the two factors.

RESULTS

For the F0 generation, analyses of variance showed a significant effect of altitude and of interaction between sex and altitude, while no effect of sex on longevity was observed (table 2a). To further understand the effect of altitude on longevity, we compared the model with sex only to the complete model with sex, altitude and interaction. This gave a global effect of altitude and sex × altitude on longevity which was highly significant (F 4, 270 = 3.54, P = 0.008).

Table 2.

Analysis of variance tables for captive cohort, F0 (a) and for F1 generation (b).

(a) Source of variance df sum sq mean sq F value P value
sex 1 3107 3107 0.79 0.373
altitude 2 30221 15111 3.87 0.022
sex × altitude 2 25196 12598 3.22 0.041
Residuals 270 1055246
(b) Source of variance df sum sq mean sq F value P value
sex 1 3087 3087 0.38 0.5386
altitude 2 170589 85294 10.48 <0.0001
sex × altitude 2 12158 6079 0.75 0.4749
Residuals 270 2198096 8141
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For the F1 generation, analysis of variance showed a strong effect of altitude, while no effect of sex and of interaction between sex and altitude was observed on longevity (table 2b).

Differences in life expectancies among populations were substantial ranging from 116 to 165 days for males and from 106 to 173 days for females (table 3). Life expectancy of F0 males showed a strong increase with increasing altitude, while no differences in life expectancy of F0 females were observed. For F1 males and females a higher life expectancy was observed at 900 m compared to 300 and 600 m.

Table 3.

Adult life expectancy (at capture for F0, at birth for F1) (days). Confidence intervals were estimated as the 2.5 and 97.5 ‰ of a bootstrap distribution re-sampled 1000 times (Efron & Tibshirani, 1993; Caswell, 2001).

generation sex

300		 Altitude (m)

600

900
F0 male 116 [101, 129] 141 [123, 159] 165 [147, 184]
female 146 [128, 162] 147 [128, 165] 148 [129, 168]
F1 male 130 [105, 154] 117 [90, 143] 165 [141, 188]
female 106 [81, 130] 113 [85, 145] 173 [147, 201]
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DISCUSSION

Our prediction of increase in lifespan with higher altitude is partly verified in this study. For field collected flies (F0) the average remaining lifespan of males monotonically increased with altitude, while the remaining lifespan of females was not influenced by the collection place. For the F1 generation, longevity of both males and females of the highest-altitude (900 m) population was longer than for the two other lower-altitude populations (300 and 600 m). As distances among sites are relatively low, gene flow among C. rosa populations may occur (Baliraine et al., 2004). However, differences in longevity among F1 populations are assumed to have a genetic component. This relationship between altitude and lifespan may be explained by the effect of temperature on reproduction. Reproductive schedules in insects are linked to temperature: lower temperature, characteristic of high-altitude sites, generally slows down reproduction. This is the case for C. rosa which show decreasing ovarian maturation rates, and therefore fecundity, with lower altitude (Duyck & Quilici, 2002). Because of the strong trade-off between reproduction and longevity, we therefore observed a longer lifespan for the high- altitude populations. Early in the 20th century, Ripley & Hepburn (1930) indeed observed that, at high altitudes in South Africa, the Natal fruit fly, was overwintering at the adult stage.

Other hypotheses could also explain such a pattern. For example different predation rates may explain variation in senescence rates (Reznick et al., 2006; Reznick et al., 2004). Populations subjected to a lower predation rate may evolve to a longer lifespan. This means that in our case study populations from the high-altitude site would have been exposed to lower predation rates. While data are lacking on adult C. rosa natural enemies, such as ants, spiders or wasps, it is likely that they might be more abundant in warm low altitude areas. In addition, larval host-fruits and adult food have been shown to effects on the life-history traits of Tephritidae, including longevity and fecundity (Brévault, Duyck & Quilici, 2008; Duyck et al., 2008). As different altitudes result in different habitats with probably different host species and adult food sources, the differential longevities among sites may be also partly explained by these factors. These different hypotheses: temperature, natural enemies, and resources may be combined in the explanation of the observed effect of altitude.

Few studies examined the effect of altitude on longevity in insect species. Contrary to our conclusions Tatar et al. (1997) showed an inverse pattern of decreasing longevity with increasing altitude in Melanoplus grasshoppers. However, this result may be due to the species studied and the place where these species have evolved to accelerated reproductive schedules that need to be carried out during summer because of severe winter conditions at the elevated sites. Our results of increased longevity with altitude are in accordance with those of Karl & Fischer (2009). Comparing populations of the butterfly Lycaena tityrus (Lycaenidae) from low and high altitudes, the authors showed an increased lifespan with higher altitude when insects were fed on a full diet. This trend of greater longevity in high-altitude populations has also been shown for Drosophila buzzatii Patterson & Wheeler, 1942 (Norry et al., 2006) and for some amphibians (Morrison & Hero, 2003; Morrison, Hero & Browning, 2004).

Contrary to our conclusions, studies on birds from a tropical warm environment show longer lifespan than for birds from a temperate cold environment (Fogden, 1972; Møller, 2007; Wiersma et al., 2007). This may be explained by the fact that, contrary to insects, birds are homeothermic organisms. In cold environments, birds likely have evolved metabolic machinery with high thermogenic capacity which may mandate a high basal metabolic rate (Wiersma et al., 2007). Møller (2007) showed that senescence rate among bird species increases with increasing latitude, and therefore with decreasing temperature. This relationship in birds is explained by the hypothesis that tropical birds have evolved life-history traits indicative of a slow rate of aging linked to a reduced basal metabolic rate (Wiersma et al., 2007).

Surprisingly, for some of the cohorts, life expectancy was longer for F0 than for mean captive lifespan of F1. A possible interpretation for this might be that adults trapped in the field (F0) were overall young and their early experience in the field was beneficial and increased their longevity. For example adults in the field may have found some nutrients that we did not give in laboratory conditions. This is in accordance with Carey et al.(2008) who showed that the lifespans of a fraction of once-wild flies would exceed the lifespans of any never-wild flies. These authors hypothesized that there is a window in the early adulthood of medfly when the presence of certain amounts or types of bacteria in its diet is important and that wild flies have access to these bacteria while reference flies in the laboratory do not, which has been shown for Drosophila (Brummel et al., 2004). Another possible explanation relates to demographic selection arguments (Vaupel & Carey, 1993). Field flies may have died easily during a certain period of time in their early life and most of the captured flies already passed that period of time. Therefore, captured F0 flies could represent a selected cohort for which all short-lived flies have already died before the beginning of the experiment. However this selection argument would change the frequency of older flies but not the absolute lifespans (see Carey et al. (2008) for a complete discussion on this point).

A significant interaction between sex and altitude on longevity has been shown for F0 generation because there is no effect of altitude on females while an increasing longevity is observed with increasing altitude in males. Differences between F0 and F1 generations may reflect differences in longevity, in age structure or both. Our data suggest that the age structure in trap (F0) is modified compared to a population at equilibrium. For example, Kouloussis et al. (2009) showed that the age structure of fruit flies may be modified by season and trapping method. An explanation for unchanged longevity for F0 females may be attributed to the response of females to the “3-lures” attractant. In other Tephritidae species, it has been observed that the response of females to various attractants depends on their physiological stage (Kendra et al., 2005; Rousse et al., 2005). Although the different female populations were coming from different habitats, their average physiological stage would be similar, and therefore, their residual lifespan under laboratory conditions not different.

Very few studies are available on the effect of altitude on longevity. Our prediction of an increase in lifespan with higher altitude has been partly verified and could invoke temperature via trade-off with reproduction. The effects of altitude variation in lifespan have theoretical implications for the understanding of lifespan evolution, but also practical implications as to the possible adaptation of ectotherms to climate warming (Tewksbury, Huey & Deutsch, 2008).

ACKNOWLEDGEMENTS

Research supported by NIA/NIH grants P01 AG022500-01 and P01 AG08761-10. Research of Jane-Ling Wang is partially supported by a NIH grant 1R01AG025218-01. We thank Mathilde HOARAU, Serge GLENAC and Jim PAYET for technical assistance and anonymous referees for helpful suggestions on the manuscript.

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