We report two important findings: (1) the positive relationship between signalling and life span (i.e. negative relationship between signalling and hazard rates); and (2) the significant difference in signalling frequency between the longest- and the shortest-lived flies early in adult life. These results support the hypothesis that intensive sexual signalling (advertisement) is an indicator of longer life span. Since males experienced similar conditions (e.g. environment, high quality food, easy accessibility to food, obtained from the same host and area) this relationship may indicate underlying genetic differences in male quality in terms of life span. Under optimum phenotypic conditions the expression of a trait such as sexual signalling is expected to be higher in fitter individuals. The high variability in signalling frequency among males in this study as well as the differences in signalling frequency between the longest- and the shortest-lived individuals underscore the above suggestion. The difference in signalling rates early in adult life between the longest- and the shortest-lived flies could be also used to predict the longest-lived individuals in the population and also to identify, early in adult life, the fittest males.
Our results that sexual signalling is positively correlated with the life span are in agreement with the recent findings by Jennions et al. (2001)
, who conducted a meta analysis and found that there is a positive relationship between sexually selected traits (such as sexual signalling) that are correlated with mating success and traits correlated with male life span, and this relationship is stronger in lekking species. Costly sexual advertisement is considered as a life history trait, which is subject to trade-offs with other components of reproductive effort, and future survival (Kokko et al. 2002
). Frequency of sexual advertisement and other secondary sexual traits are condition depended and increases with high genetic viability (Rowe and Houle 1996
). Theory predicts that if a trait such as sexual signalling in our case is costly its size and life span (viability) should be negatively correlated (Kotiaho et al. 1999
). However, a positive correlation between life span and the size of the trait is anticipated if the expression of the trait depends on the phenotypic condition of the individual such that the costs of the trait are less for individuals in good conditions than for individuals in poor condition (Kotiaho et al. 1999
and references therein). Variation in the ability to bear the cost may reflect underlying differences in male quality. In general males of higher quality are more likely to be in better condition and expected to express higher intensity of the respective trait.
Sexual signalling commits medfly males to a high energetic investment, there is a remarkable metabolic cost in biosynthesis and emission of sex pheromone, and only males that can forage successfully can exhibit this behaviour in nature (Warburg and Yuval 1997
; Yuval et al. 1998
). Here we found that sexual signalling varies a lot among individuals under optimum diet conditions in the laboratory. Therefore, other factors besides successful foraging may be important determinants of signalling frequency. Our results (non-existence of a negative correlation between sexual signalling and life span) show that sexual signalling in the absence of other sexual activities has no obvious effect on male life span under laboratory (predation-free) conditions. However, experimental manipulations in which signalling rates would be disentangled from condition need to be done to address more directly questions regarding the cost of sexual signalling. Metabolic cost, which is increased by courtship activity, is probably important in reducing life span in male Drosophila melanogaster
(Cordts and Partridge 1996
). Reduced life span due to increased sexual activities might also be related to altered hormonal status in males. Participation in leks and frequent signalling in nature might also be costly in terms of reduced viability since it reduces male opportunities for foraging and exposes them to high predation risk (Hendrichs et al. 1991
; Hendrichs and Hendrichs 1998
). The importance of predation and food availability as mortality factors in wild populations has not been investigated in detail in this fly. More field work is needed to clarify issues related with male survival in the wild.
Although females cannot assess male quality based on frequency of signalling, males that signal at higher rates enjoy higher reproductive success (Shelly 2000
). There is a direct relationship between signalling frequency, female attraction, number of courtships performed and matings achieved (Whittier et al. 1994a
). This indicates that signalling frequency may be sexually selected, most probably through male-male competition. The ability of males in lekking or other mating systems to remain reproductively active for a long period is well appreciated as important in increasing the number of matings (Andersson 1994
; Andersson and Iwasa 1996
). Sexual signalling is universal in this fly because all males exhibited this behaviour (; see also Whittier et al. 1994a
). It is also a large time investment for the individuals since signalling was exhibited on >80% of days of the total life span. Nonetheless, the proportion of non-mating males, estimated in short term studies over an approximately 1-week period (early in adult life) is usually high (≈40–55%) (Shelly 2000
; Whittier et al. 1994a
). Our results indicate that signalling frequency remained almost constant throughout the life span of individuals and dropped only approximately 1 week before death. We can therefore suggest that high signalling rates in medfly males may confer a lifetime mating advantage to individuals providing a large fitness benefit. However, this suggestion should be tested experimentally in order to elucidate whether mating performance, not just signalling frequency, remains constant throughout the life span, and whether old males can compete with younger ones in attracting females and achieving matings. On the other hand, it is not clear whether females gain benefits of mating with an attractive male that signals frequently. In fact, individual females that mate with males with high mating rates (attractive males) do not have sons with higher attractiveness and mating success (Whittier and Kaneshiro 1995
). However, it is not known whether their sons experience higher survival probabilities and higher lifetime mating success through longer reproductive life spans.
Lifetime data of individual flies provide insight into inter-fly variation in sexual signalling, allow between-fly comparisons in lifetime levels of signalling rates, and reveal compositional influences on the cohort averages (Carey et al. 1998
). They also provide insights into intra-fly differences in signalling rates connecting the intensity of expression early and late in life. The results of this study show that signalling, and probably other behaviours, have age-specific properties that define the sexually active life span of individuals, which is a major component of male fitness in lekking species. The sexually active life span as it is indicated by signalling is almost 2 weeks shorter than the total life span, and the frequency of signalling remains constantly high for individuals during most of this period. After peak rates have been assumed, a substantial decrease and cessation in daily signalling rates can be used as an index of high mortality risk. In fact, as medfly males approach death, they spend a progressively increasing amount of time in a supine position, which indicates an irreversible morbidity condition and predicts death (Papadopoulos et al. 2002
). Sexual signalling and supine behaviour can be used to determine morbidity dynamics and its underlying causes in male medflies, also providing reliable behavioural biomarkers of aging. A biomarker of aging is a behavioural or biological parameter of an organism that can, either alone or in some multivariate composite, better predict functional capacity and/or mortality risk at some later age than the chronological age (Markowska and Breckler 1999
). Other behavioural adjustments to increase of the mortality risk, such as alternations of the reproductive behaviour of parasitic wasps (Roitberg et al. 1993
), can provide important indicators of individual and cohort life expectancy.
Because studies of different types of insect behaviour such as foraging, mating, and reproductive behaviours have traditionally focused on young or middle-aged individuals, little is known about insect behaviour in older individuals or the relationship of different behaviours at young ages to life history traits in older individuals (Alcock 1997
). Likely reasons for ignoring the behaviour of the elderly in nature is because life table information in field populations suggest that most individuals in nature die young, and that the evolutionary theory of aging (Kirkwood and Austad 2000
; Partridge 2001
suggests that older individuals contribute little to fitness. Behavioural research on older individuals not only provides a more complete account of behavioural dynamics during all stages of a species’ life course, it also provides data and context for testing evolutionary theories of aging and organisational framework for interdisciplinary research in life history theory. Behavioural traits, not only birth and death rates, can also be characterised as age-specific intensity as we show in the current study. Age-specific behavioural data can then be used to test theories about the cost of reproduction in the context of mating, signalling, and courting as well as juxtaposed with changes in other life history traits.