Therésa M. Jones

The role of chemical communication in mate choice

Chemical signals are omnipresent in sexual communication in the vast majority of living organisms. The traditional paradigm was that their main purpose in sexual behaviour was to coordinate mate and species recognition and thus pheromones were conserved in structure and function. In recent years, this view has been challenged by theoretical analyses on the evolution of pheromones and empirical reports of mate choice based on chemical signals. The ability to measure precisely the quantity and quality of chemicals emitted by single individuals has also revealed considerable individual variation in chemical composition and release rates, and there is mounting evidence that prospecting mates respond to this variation. Here, we review the evidence for pheromones as indicators of mate quality and examine the extent of their use in individual mate assessment. We begin by briefly defining the levels of mate choice – species recognition, mate recognition and mate assessment. We then explore the degree to which pheromones satisfy the key criteria necessary for their evolution and maintenance as cues in mate assessment; that is, they should exhibit variation across individuals within a sex and species; they should honestly reflect an individual’s quality and thus be costly to produce and/or maintain; they should display relatively high levels of heritability. There is now substantial empirical evidence that pheromones can satisfy all these criteria and, while measurements of the actual metabolic cost of pheromone production remain to some degree lacking, trade‐offs between pheromone production and various fitness‐related characters such as growth rate, immunocompetence and longevity have been reported for a range of species. In the penultimate section, we outline the growing number of studies where the consequences of chemical‐based mate assessment have been investigated, specifically focussing on the reported direct and genetic benefits accrued by the receiver. Finally, we highlight potential areas for future research and in particular emphasise the need for interdisciplinary research that combines exploration of chemical, physiological and behavioural processes to further our understanding of the role of chemical cues in mate assessment.

Adaptive female choice for middle–aged mates in a lekking sandfly

Most theoretical models of age–related mate choice predict that females should prefer older males because they have proven survival ability. An alternative view is that older males represent inferior mates because of negative genetic correlations between early and late fitness components, or because older males have traded off longevity against other fitness components, have accumulated deleterious germ–line mutations, or are less well adapted to current conditions than more recently born individuals. While numerous studies have reported female choice for older males, few have explicitly examined the fitness consequences of such a preference. We present evidence from a lekking sandfly, Lutzomyia longipalpis , showing that choosy females discriminate against older males and gain a fitness benefit from their choice. When permitted free choice from an aggregation consisting of males aged zero to two days (young), four to six days (middle–aged) and eight to ten days (old), females preferentially mated with middle–aged males, but all measures of female reproductive success were independent of male age. In contrast, when a second set of females was randomly assigned single virgin males of known age, the eggs of those paired to old mates exhibited lower hatching success than the eggs of females mated to young or middle–aged males. These results suggest that females avoid mating with older males because they represent poorer quality mates. Age–related differences in male quality may have a genetic basis, but could equally well arise through a phenotypic decline in sperm quality or sperm transfer ability with male age. The lack of evidence of female discrimination against older males from other studies may be because these did not explore the reproductive success of the full age range of males.

The role of male age, sperm age and mating history on fecundity and fertilization success in the hide beetle.

Models of age–related mate choice predict female preference for older males as they have proven survival ability. However, these models rarely address differences in sperm age and male mating history when evaluating the potential benefits to females from older partners. We used a novel experimental design to assess simultaneously the relative importance of these three parameters in the hide beetle, Dermestes maculatus. In a two–part experiment we first explored age–related male mating success and subsequently examined the consequences of male age, sperm age and male mating history on female fecundity and fertilization success. In a competitive mating environment, intermediate–age males gained significantly higher mating success than younger or older males. To test the consequences for females of aged–related male mating success, a second set of females were mated to males varying in age (young, intermediate–age and old), in numbers of matings and in timing of the most recent mating. We found that male age had a significant impact on female fecundity and fertilization success. Females mated to intermediate–age males laid more eggs and attained consistently higher levels of fertilization success than females with young and old mates. A males previous mating history determined his current reproductive effort; virgin males spent longer in copula than males with prior mating opportunities. However, differences in copulation duration did not translate into increased fecundity or fertilization success. There was also little evidence to suggest that fertilization success was dependent on the age of a males sperm. The experiment highlights the potential direct benefits accrued by females through mating with particular aged males. Such benefits are largely ignored by traditional viability models of age–related male mating success.

Fisherian flies: benefits of female choice in a lekking sandfly

We experimentally investigated the fitness consequences of female mate choice in order to test the relative importance of three competing but non–exclusive hypotheses for the maintenance of pronounced female mating preferences on leks: that females benefit directly; that they gain indirect Fisherian benefits by producing more attractive sons; or that they benefit indirectly because preferred males possess ‘good genes’ that confer increased viability on their sons and daughters. We allowed lekking female sandflies, Lutzomyia longipalpis, to choose between males of varying attractiveness to females, and monitored the consequences for their own survival and reproductive success as well as for their offspring. In contrast to the predictions of the direct–benefits model, we found no clear sire effect on the fecundity or survival of the females themselves; females mating with more attractive males did survive longer after oviposition, but never long enough to undertake a second batch of egg laying. We also found no evidence that females gained good–genes benefits in terms of enhanced offspring survival. However, we did find that generally attractive males fathered sons who were then chosen when they in turn formed leks. Although not completely precluding other benefits, our results indicate that Fisherian benefits are at least partly responsible for maintaining female choice at L. longipalpis leks. These findings indicate the importance of testing all putative benefits concurrently in exploring the maintenance of female mate choice.

A role for pheromones in mate choice in a lekking sandfly.

There is increasing evidence to suggest that pheromone-mediated communication may play an important role in mate choice in many insects. We investigated the possible role of pheromones in mate choice in the lekking sandfly, Lutzomyia longipalpis, and explored whether males or females display any behavioural traits that predict patterns of male mating success. Pairs of virgin males were introduced into a small mating chamber and allowed to interact for approximately 10 min prior to the introduction of a single virgin female. The trial continued until the female copulated with one of the males. We recorded trials on video for later analysis. After a successful copulation, we determined the quantity of pheromone remaining in the glands of both males and measured the size of the pheromone glands and tergites. We corrected behaviours and measurements for body size (tergite width). Mated males had significantly more pheromone present in their glands after a trial than unmated males. Males differed in how much time they invested in wing fanning. Members of each pair of males spent similar amounts of time wing fanning but mated males and males with more residual pheromone spent more time wing fanning than their counterparts throughout the trial. The time spent wing fanning and the amount of residual pheromone were not correlated, however. A males ability to win fights did not relate to his reproductive success. Finally, a female was equally likely to wing-fan directly at, or walk away from, either male in a given pair. The possible relationships between the amount of pheromone released and the residual pheromones left in the glands, and the level of male wing fanning and pheromone productivity, are discussed. Copyright 1998 The Association for the Study of Animal Behaviour.

A potential cost of monandry in the lekking sandfly Lutzomyia longipalpis

Multiple mating by females is a subject of considerable controversy. In some species, however, females appear to mate only once, and the potential costs and benefits of this behavior are equally intriguing. When male mating success is highly skewed, monandrous females potentially risk mating with a sperm depleted male. In lek-breeding species, a male may gain up to 80% of available matings, yet few studies have explored whether these highly successful males suffer sperm depletion. These points are investigated in a series of laboratory experiments on the lekking sandfly, Lutzomyia longipalpis. It is shown that females may actively reject males prior to and after genital contact and that mated females do not remate within a single egg-laying cycle regardless of the refractory period between the first and subsequent matings. Males mate multiply and suffer from the effects of sperm depletion after their fifth copulation. Despite this, they continue to court and copulate females with equal vigor and females do not appear to detect sperm-depleted males: they lay similar numbers of eggs irrespective of the number of females their mate has previously copulated with. The implications of a single mating for L. longipalpis females in natural and laboratory leks are discussed.

Cost of pheromone production in a lekking Drosophila

‘Sex pheromones’ are most commonly seen as mate attraction signals. However, there is growing evidence that chemical signals may also advertise mate quality. Theory predicts that for mate quality signals to be reliable they should be costly, a mechanism that is likely to drive condition-dependent expression of the signal in question. We investigated the relation between pheromone production and life span in Drosophila grimshawi, a lekking fruit fly where males deposit pheromones on the lekking arena. We manipulated pheromone production by subjecting males to another male, a female or no companion twice a week for the duration of their adult lives. We found that long-lived males deposited pheromones for a greater proportion of their lives across treatments. Males that met other males, rather than females or no flies, also deposited pheromones for a greater proportion of their lives. However, this greater investment seemed to be costly since these males also had shorter life spans, presumably as a result of increased pheromone production. Thus, our results support the notion that pheromone production may act as an honest signal of quality. Furthermore, we show that the pheromone has multiple functions and that male D. grimshawi appear to adjust their investment in pheromone production in relation to their social environment.

Age-dependent trade-offs between immunity and male, but not female, reproduction.

Immune function is costly and must be traded off against other life-history traits, such as gamete production. Studies of immune trade-offs typically focus on adult individuals, yet the juvenile stage can be a highly protracted period when reproductive resources are acquired and immune challenges are ubiquitous. Trade-offs during development are likely to be important, yet no studies have considered changes in adult responses to immune challenges imposed at different stages of juvenile development. By manipulating the timing of a bacterial immune challenge to the larvae of the cotton bollworm moth, we examined potential trade-offs between investment into immunity at different stages of juvenile development (early or late) and subsequent adult reproductive investment into sperm or egg production. Our data reveal an age-dependent trade-off between juvenile immune function and adult male reproductive investment. Activation of the immune response during late development resulted in a reduced allocation of resources to eupyrene (fertilizing) sperm production. Immune activation from the injection procedure itself (irrespective of whether individuals were injected with an immune elicitor or a control solution) also caused reproductive trade-offs; males injected early in development produced fewer apyrene (nonfertilizing) sperm. Contrary to many other studies, our study demonstrates these immune trade-offs under ad libitum nutritional conditions. No trade-offs were observed between female immune activation and adult reproductive investment. We suggest the differences in trade-offs observed between male sperm types and the absence of reproductive trade-offs in females may be the result of ontogenetic differences in gamete production in this species. Our data reveal developmental windows when trade-offs between immune function and gametic investment are made, and highlight the importance of considering multiple developmental periods when making inferences regarding the fundamental trade-offs expected between immune function and reproduction.

Melatonin: a possible link between the presence of artificial light at night and reductions in biological fitness

The mechanisms underpinning the ecological impacts of the presence of artificial night lighting remain elusive. One suspected underlying cause is that the presence of light at night (LAN) supresses nocturnal production of melatonin, a key driver of biological rhythm and a potent antioxidant with a proposed role in immune function. Here, we briefly review the evidence for melatonin as the link between LAN and changes in behaviour and physiology. We then present preliminary data supporting the potential for melatonin to act as a recovery agent mitigating the negative effects of LAN in an invertebrate. Adult crickets (Teleogryllus commodus), exposed to constant illumination, were provided with dietary melatonin (concentrations: 0, 10 or 100 µg ml−1) in their drinking water. We then compared survival, lifetime fecundity and, over a 4-week period, immune function (haemocyte concentration, lysozyme-like and phenoloxidase (PO) activity). Melatonin supplementation was able only partially to mitigate the detrimental effects of LAN: it did not improve survival or fecundity or PO activity, but it had a largely dose-dependent positive effect on haemocyte concentration and lysozyme-like activity. We discuss the implications of these relationships, as well as the usefulness of invertebrates as model species for future studies that explore the effects of LAN.

Large spermatophores reduce female receptivity and increase male paternity success in the almond moth, Cadra cautella.

The size of a males reproductive investment may have profound consequences for female mating frequency and male fitness. Male ejaculate size may affect female fecundity and fertility, while large ejaculates may confer an advantage for males in both avoiding and engaging in sperm competition. We explored experimentally the effect of male ejaculate size on female receptivity and male fertilization success, in the largely monandrous almond moth. Females received either a large or small first spermatophore, and were then given the opportunity to remate with another male that also provided a large or small ejaculate. We examined the effect of spermatophore size on female postmating receptivity, likelihood of remating and reproductive output. For males, we examined the effect that spermatophore size and mating order had on subsequent paternity success. Females that received a small first ejaculate were both more likely to remate (with mated males) and remated sooner than females that received a large first ejaculate. Furthermore, females that remated were also more likely to commence calling behaviour following their first mating, but there were no effects of spermatophore size on female reproductive output. For a male, however, if his female remated, the size of the spermatophore he transferred had important fitness consequences. Second-mating males suffered a paternity cost when competing against a rival that provided a large spermatophore. We propose that the enlarged spermatophore transferred by virgin males explains the low remating rate in this species, and may suggest a more polyandrous past for the almond moth, potentially shaped by sexual conflict.