Evolutionary genetics of Drosophila ananassae: evidence for trade-offs among several fitness traits

Correlated responses to bi‐directional selection on thorax length, examined on several life‐history traits and chromosome inversion polymorphisms, have revealed apparent novel trade‐offs in Drosophila ananassae. We provide evidence of trade‐offs between hatching time and pupal period, pupal period and egg‐pupa development time, and pupal period and larval development time (LDT). Body size shows positive correlations with ovariole number, LDT and DT (egg–fly). We provide evidence of sexual dimorphism for trade‐offs between longevity and body size and starvation and longevity in females only. Trade‐offs between wing/thorax (W/T) ratio and longevity, W/T ratio and starvation, and DT (egg‐ fly) and longevity are evident in males only. Sexual dimorphism is also evident for inversion polymorphism with body size and longevity. A longevity assay suggests that low line females outlived high line females whereas high line males outlived low line males. The mean longevity in males is negatively correlated with the 2L‐ST and 3R‐ST arrangement frequencies whereas the 3L‐ST arrangement frequency is positively correlated with the mean longevity in males but opposite arrangements are found in females. Absolute starvation resistance is negatively correlated with 2L‐ST and 3R‐ST chromosome arrangements and results in a trade‐off between longevity and absolute starvation resistance in females. Analyses of fecundity, hatchability, and viabilities based on age intervals in both G₁₀ and G₁₃ suggest that the early reproduction is favoured in D. ananassae. The productivity percentage is highest in the high line and there is no effect of late reproduction on it. Overall, we provide some unravelled trade‐offs and striking sex differences, which may help in understanding the life‐history evolution of the species. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 90 , 669–685.     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.     

Effects of sugar feeding on carbohydrate and lipid metabolism in a parasitoid wasp

Lifetime patterns of carbohydrate and lipid metabolism were compared in starved and sucrose‐fed adults of the parasitoid Macrocentrus grandii (Goidanich) (Hymenoptera: Braconidae). As expected, sucrose‐fed individuals lived longer than did starved individuals. Macrocentrus grandii males and females eclosed with levels of simple storage sugars (presumably primarily trehalose) and glycogen that were below maximum levels recorded from sucrose‐fed parasitoids. Both of these nutrients dropped to very low levels in starved individuals within 4 days post‐emergence and were maintained at high levels in sucrose‐fed individuals throughout their lives. Lipid reserves at emergence represented the highest lipid levels for both sexes in the two diet treatments, with levels declining over the lifetimes of males and females from both diet treatments. Our results therefore suggest that dietary sucrose is used to synthesize trehalose and glycogen, but not lipids in M. grandii. Also, in contrast to the patterns observed for the simple sugars and glycogen, lipid levels in starved individuals did not drop below levels observed in sugar‐fed individuals. The average number of mature eggs carried by females at emergence was 33 and increased to approximately 85 in sucrose‐fed and 130 in starved females by the age of 5 d in the absence of hosts. The egg maturation rate was therefore higher in starved than in sugar‐fed females. Potential explanations for this unexpected result are discussed.     

Evolution of starvation resistance in an invasive insect species,Aethina tumida (Coleoptera: Nitidulidae)

Starvation resistance, or the ability to survive periods without food, can shed light on selection pressure imposed by food scarcity, including chances to invade new regions as a result of human transport. Surprisingly, little information is known about starvation resistance for invasive insect species. Given that native and invasive populations differ in starvation resistance, this would suggest different selection scenarios and adaptive shifts fostering invasion success. Here, we show striking differences in starvation resistance of adult small hive beetles Aethina tumida (SHB) between native and invasive populations. In the laboratory, starvation resistance of freshly emerged laboratory‐reared and field‐collected adult females and males was evaluated in the beetle's native African range and in their invasive North American range. SHB in their native African range survived longer than SHB in their invasive North American range. Across ranges, females survived longer than males. Field‐collected SHB survived in Africa longer than freshly emerged ones, but not in the invasive range. This suggests no selection for starvation resistance in the invasive range, possibly due to differences between African and European‐derived honey bee hosts facilitating a trade‐off scenario between reproduction and starvation resistance. The ability of adult females to survive up to two months without food appears to be one factor contributing to the invasion success of this species. Assuming food availability is usually high in the invasive ranges, and trade‐offs between starvation resistance and fecundity/reproduction are common, it seems as if selection for starvation resistance during transport could set up potential trade‐offs that enhance reproduction after invasion. It would be interesting to see if this is a possible general pattern for invasive insect species.     

Selection on learning performance results in the correlated evolution of sexual dimorphism in life history

The evolution of learning can be constrained by trade‐offs. As male and female life histories often diverge, the relationship between learning and fitness may differ between the sexes. However, because sexes share much of their genome, intersexual genetic correlations can prevent males and females from reaching their sex‐specific optima resulting in intralocus sexual conflict (IaSC). To investigate if IaSC constraints sex‐specific evolution of learning, we selected Caenorhabditis remanei nematode females for increased or decreased olfactory learning performance and measured learning, life span (in mated and virgin worms), reproduction, and locomotory activity in both sexes. Males from downward‐selected female lines had higher locomotory activity and longer virgin life span but sired fewer progeny than males from upward‐selected female lines. In contrast, we found no effect of selection on female reproduction and downward‐selected females showed higher locomotory activity but lived shorter as virgins than upward‐selected females. Strikingly, selection on learning performance led to the reversal of sexual dimorphism in virgin life span. We thus show sex‐specific trade‐offs between learning, reproduction, and life span. Our results support the hypothesis that selection on learning performance can shape the evolution of sexually dimorphic life histories via sex‐specific genetic correlations.     

Reproduction-longevity trade-offs reflect diet, not adaptation

A tenet of life history evolution is that allocation of limited resources results in trade‐offs, such as that between reproduction and lifespan. Reproduction and lifespan are also influenced proximately by differences in the availability of specific nutrients. What is unknown is how the evolution of the ability to use a nutritionally novel diet is reflected in this fundamental trade‐off. Does the evolution of the ability to use a nutritionally novel food maintain the trade‐off in reproduction and longevity, or do the proximate effects of nutrition alter the adapted trade‐off? We tested this by measuring trade‐offs in male milkweed bugs, Oncopeltus fasciatus, fed either an adapted diet of sunflower or the ancestral diet of milkweed. Sunflower‐fed males lived longer but invested less in reproduction, both in mating and fertility. Milkweed‐fed males invested in both mating and fertility at the expense of survival. The evolution of an expanded diet was not constrained by the existing trade‐off, but instead was accompanied by a different trade‐off between reproduction and longevity. We suggest that this occurs because diets differ in promoting germ line development or longevity.     

Methyl eugenol effects on Bactrocera dorsalis male total body protein,reproductive organs and ejaculate

Methyl eugenol (ME) and inclusion of protein into the adult diet increase the mating competitiveness of the Oriental fruit fly, Bactrocera dorsalis (Hendel). Exposing males to ME or protein is a promising post‐teneral treatment for males being released in the sterile insect technique (SIT). However, the effect of this post‐teneral treatment on male reproductive organs or the male ejaculate is unknown. During mating, males transfer sperm and accessory gland products (AGPs) to females and these compounds are reported to modulate female sexual inhibition. We studied the impact of male exposure to ME and a yeast hydrolysate (YH) diet on the protein reserves of males, male reproductive organ size, and the male ejaculate through sperm and AGPs. We show that males exposed to ME regardless of access to YH accumulated a greater amount of whole body protein. Males fed on YH also had increased total body protein and had bigger reproductive organs than YH‐deprived males, but no apparent effect of ME exposure was observed on reproductive organ size. Females stored less sperm when mated with males fed on YH and ME compared to males not fed on ME. YH and ME had no effect on male AGPs. Females injected with AGPs of males fed on YH and exposed to ME were just as likely to mate as females injected with AGPs of non‐treated males. However, females injected with AGPs of males exposed to ME mated faster than females injected with AGPs of non‐exposed males. We conclude that while exposure to ME increases male copulatory success and protein reserves in the male body, there seem to be some potential trade‐offs such as lower sperm stored by females. We discuss our results in terms of pre‐release protocols that may be used for B. dorsalis in SIT application.     

Costs of intersexual conflict in the isopod Idotea baltica

In sexual reproduction one sex can increase its reproductive success at the cost of the other, a situation known as intersexual conflict. In the marine isopod Idotea baltica, males guard females before copulation. The guarding phase is preceded by struggles as females resist males’ attempts to initiate guarding. We determined whether the struggle and/or mate‐guarding result in fitness costs in the form of decreasing fecundity and lower levels of the energy storage compounds, glycogen and lipids. Females that underwent the period of struggles with males had decreased glycogen levels compared with females maintained alone. No such cost was found for males. Females guarded by a male also had smaller eggs than females that were not guarded. Thus the intersexual conflict, imposed by the fitness maximization strategy of the males, gave rise to both a fecundity cost and an energetic cost for females. The fecundity cost confirms the existence of intersexual conflict in I. baltica. This cost is shared by males, suggesting that the intersexual conflict restrains the reproductive output of both sexes.     

THE CONTRIBUTION OF SPONTANEOUS MUTATIONS TO THERMAL SENSITIVITY CURVE VARIATION IN DROSOPHILA SERRATA

Many traits studied in ecology and evolutionary biology change their expression in response to a continuously varying environmental factor. One well‐studied example are thermal performance curves (TPCs); continuous reaction norms that describe the relationship between organismal performance and temperature and are useful for understanding the trade‐offs involved in thermal adaptation. We characterized curves describing the thermal sensitivity of voluntary locomotor activity in a set of 66 spontaneous mutation accumulation lines in the fly Drosophila serrata. Factor‐analytic modeling of the mutational variance–covariance matrix, M , revealed support for three axes of mutational variation in males and two in females. These independent axes of mutational variance corresponded well to the major axes of TPC variation required for different types of thermal adaptation; “faster‐slower” representing changes in performance largely independent of temperature, and the “hotter‐colder” and “generalist‐specialist” axes, representing trade‐offs. In contrast to its near‐absence from standing variance in this species, a “faster‐slower” axis, accounted for most mutational variance (75% in males and 66% in females) suggesting selection may easily fix or remove these types of mutations in outbred populations. Axes resembling the “hotter‐colder” and “generalist‐specialist” modes of variation contributed less mutational variance but nonetheless point to an appreciable input of new mutations that may contribute to thermal adaptation.     

Sexual selection shapes development and maturation rates in Drosophila

Explanations for the evolution of delayed maturity usually invoke trade‐offs mediated by growth, but processes of reproductive maturation continue long after growth has ceased. Here, we tested whether sexual selection shapes the rate of posteclosion maturation in the fruit fly Drosophila melanogaster. We found that populations maintained for more than 100 generations under a short generation time and polygamous mating system evolved faster posteclosion maturation and faster egg‐to‐adult development of males, when compared to populations kept under short generations and randomized monogamy that eliminated sexual selection. An independent assay demonstrated that more mature males have higher fitness under polygamy, but this advantage disappears under monogamy. In contrast, for females greater maturity was equally advantageous under polygamy and monogamy. Furthermore, monogamous populations evolved faster development and maturation of females relative to polygamous populations, with no detectable trade‐offs with adult size or egg‐to‐adult survival. These results suggest that a major aspect of male maturation involves developing traits that increase success in sexual competition, whereas female maturation is not limited by investment in traits involved in mate choice or defense against male antagonism. Moreover, rates of juvenile development and adult maturation can readily evolve in opposite directions in the two sexes, possibly implicating polymorphisms with sexually antagonistic pleiotropy.     

Opposing effects on glutathione and reactive oxygen metabolites of sex,habitat, and spring date,but no effect of increased breeding density in great tits (Parus major)

Oxidative stress (i.e., more oxidants than antioxidants) has been proposed as a proximate currency in life‐history trade‐offs, which if studied in an ecological setting allow a more realistic perspective on the origin and evolution of trade‐offs. Therefore, the aim here was to investigate the impact of ecological and individual factors for variation in markers of oxidative stress using both experimental and correlational data. Total glutathione (tGSH), oxidized glutathione (GSSG), plasma antioxidant capacity (OXY), and plasma‐reactive oxygen metabolites (ROM) were measured in more than 700 breeding great tits (Parus major). The main results revealed a pronounced sex difference, with females having lower ROM and OXY, but higher tGSH compared with males. In addition, birds breeding in the evergreen areas had higher tGSH compared with those in the deciduous habitat, but the experimentally manipulated breeding density had no significant effect on any of the redox markers. Independent of the sex differences, the larger the reproductive investment the lower the ROM of both males and females. Taken together, the extracellular markers – ROM and OXY – revealed similar results and were highly correlated. Interestingly, the direction of their effects was in the opposite direction to the endogenously synthesized tGSH and GSSG. This highlights the need to combine extracellular markers with endogenously synthesized antioxidants to understand its implications for the origin and evolution of trade‐offs in an ecological setting.     

Experimental manipulation reveals a trade‐off between weapons and testes

Theory predicts a trade‐off between sexually selected weapons used to secure mates and post‐copulatory traits used to maximize fertilization success. However, individuals that have a greater capacity to acquire resources from the environment may invest more in both pre‐ and post‐copulatory traits, and trade‐offs may not be readily apparent. Here, we manipulate the phenotype of developing individuals to examine allocation trade‐offs between weapons and testes in Mictis profana (Hemiptera: Coreidae), a species where the hind legs are sexually selected weapons used in contests over access to females. We experimentally prevented males from developing weapons by inducing them to autotomize their hind legs before the final moult to adulthood. We compared trait expression in this group to males where autotomy was induced in the mid‐legs, which are presumably not under sexual selection to the same extent. We found males without weapons invested proportionally more in testes mass than those with their mid‐legs removed. Males that developed to adulthood without weapons did not differ from the mid‐leg removal group in other traits potentially under precopulatory sexual selection, other post‐copulatory traits or naturally selected traits. In addition, a sample of adult males from the same population in the wild revealed a positive correlation between investment in testes and weapons. Our study presents a critical contribution to a growing body of literature suggesting the allocation of resources to pre‐ and post‐copulatory sexual traits is influenced by a resource allocation trade‐off and that this trade‐off may only be revealed with experimental manipulation.     

Laboratory evolution of longevity in the bean weevil (Acanthoscelides obtectus)

In this study we examined the effects of long-term selection on early and late reproduction in the bean weevil. The pure lines and the hybrids between the lines within a selection regime were compared for longevity, early and late female fecundity, male mating ability, pre-adult developmental time and wet adult weight. Comparison of hybrid with pure lines provided some evidence for inbreeding despression in the lines from both selection regimes. We found that virgin and mated adults of both sexes from the “old” lines lived longer than “young” line beetles. Comparisons of the hybrid “young” with hybrid “old” lines revealed a trade-off between early and late fecundity of females. For noncompetitive mating ability of males there was no difference between the lines with different rates of senescence when the males were young. But, when the males were older, beetles from the lines selected for delayed senescence expressed superior mating ability. In addition, the “old” line beetles take longer to develop and are heavier than those from “young” line beetles. Although these data suggest that shorter pre-adult developmental time may imply more rapid senescence, there is the possibility of inadvertent selection for rapid development in the “young” lines and this complicates the interpretation of the observed trade-off between the pre-adult and adult performances.     

Effects of pathogen exposure on life‐history variation in the gypsy moth (Lymantria dispar)

Investment in host defences against pathogens may lead to trade‐offs with host fecundity. When such trade‐offs arise from genetic correlations, rates of phenotypic change by natural selection may be affected. However, genetic correlations between host survival and fecundity are rarely quantified. To understand trade‐offs between immune responses to baculovirus exposure and fecundity in the gypsy moth (Lymantria dispar), we estimated genetic correlations between survival probability and traits related to fecundity, such as pupal weight. In addition, we tested whether different virus isolates have different effects on male and female pupal weight. To estimate genetic correlations, we exposed individuals of known relatedness to a single baculovirus isolate. To then evaluate the effect of virus isolate on pupal weight, we exposed a single gypsy moth strain to 16 baculovirus isolates. We found a negative genetic correlation between survival and pupal weight. In addition, virus exposure caused late‐pupating females to be identical in weight to males, whereas unexposed females were 2–3 times as large as unexposed males. Finally, we found that female pupal weight is a quadratic function of host mortality across virus isolates, which is likely due to trade‐offs and compensatory growth processes acting at high and low mortality levels, respectively. Overall, our results suggest that fecundity costs may strongly affect the response to selection for disease resistance. In nature, baculoviruses contribute to the regulation of gypsy moth outbreaks, as pathogens often do in forest‐defoliating insects. We therefore argue that trade‐offs between host life‐history traits may help explain outbreak dynamics.     

Close‐kin mating,but not inbred parents,reduces hatching rates and offspring quality in a threatened tortoise

Inbreeding depression, the reduction in fitness due to mating of related individuals, is of particular conservation concern in species with small, isolated populations. Although inbreeding depression is widespread in natural populations, long‐lived species may be buffered from its effects during population declines due to long generation times and thus are less likely to have evolved mechanisms of inbreeding avoidance than species with shorter generation times. However, empirical evidence of the consequences of inbreeding in threatened, long‐lived species is limited. In this study, we leverage a well‐studied population of gopher tortoises, Gopherus polyphemus, to examine the role of inbreeding depression and the potential for behavioural inbreeding avoidance in a natural population of a long‐lived species. We tested the hypothesis that increased parental inbreeding leads to reduced hatching rates and offspring quality. Additionally, we tested for evidence of inbreeding avoidance. We found that high parental relatedness results in offspring with lower quality and that high parental relatedness is correlated with reduced hatching success. However, we found that hatching success and offspring quality increase with maternal inbreeding, likely due to highly inbred females mating with more distantly related males. We did not find evidence for inbreeding avoidance in males and outbred females, suggesting sex‐specific evolutionary trade‐offs may have driven the evolution of mating behaviour. Our results demonstrate inbreeding depression in a long‐lived species and that the evolution of inbreeding avoidance is shaped by multiple selective forces.     

Sexual dimorphism and growth trade‐offs in Blue Tit Cyanistes caeruleus nestlings

The outcome of sibling competition for food is often determined by variation in body size within the brood and involves trade‐offs; traits that enhance competitive ability within the nest may be developed at the expense of traits that enable effective flight at fledging, or vice versa. We quantified growth of skeletal, body mass and feather traits in male and female Blue Tit Cyanistes caeruleus nestlings. Males were significantly heavier, had longer tarsi and tended to have greater head–bill lengths than females, whereas females were similar to males in wing flight feather growth. These differences in growth may result from sexual differences in selection of the traits. Females are likely to prioritize feather growth to facilitate synchronized fledging with the rest of the brood, and to enhance escape from predators. We suggest that males are heavier and develop longer tarsi because body size is an important determinant of male reproductive success.     

Variation in energy reserves and role of body size in the mating system of Anopheles gambiae

Anopheles gambiae mates in flight. Males gather at stationary places at sunset and compete for incoming females. Factors that account for male mating success are not known but are critical for the future of any genetic control strategy. The current study explored variations in nutritional reserves (sugars, glycogen, lipids, and proteins) in wild‐caught swarming and resting males and evaluated the effect of body size and wing symmetry on male mating success. Our results showed that glycogen and sugar reserves are mobilized for flight. Males consume proportionally 5.9‐fold as much energy derived from sugars in swarming activities than when they are at rest. Mated males were on average bigger than unmated ones (P<0.0001). A strong correlation between the left and right wings in both mated and unmated males was found and additional analysis on fluctuating asymmetry did not show any indication of mated males being more symmetrical than unmated ones. The distribution of wing size of mated males was focused around a central value, suggesting that intermediate size of males is advantageous in the An. gambiae mating system. The results are discussed in the context of sexual selection.     

EXPERIMENTAL EVOLUTION OF FEMALE TRAITS UNDER DIFFERENT LEVELS OF INTERSEXUAL CONFLICT IN DROSOPHILA MELANOGASTER

A number of studies have documented the evolution of female resistance to mate‐harm in response to the alteration of intersexual conflict in the populations. However, the life‐history consequence of such evolution is still a subject of debate. In this study, we subjected replicate populations of Drosophila melanogaster to different levels of sexual conflict (generated by altering the operational sex ratio) for over 45 generations. Our results suggest that females from populations experiencing higher level of intersexual conflict evolved increased resistance to mate‐harm, in terms of both longevity and progeny production. Females from the populations with low conflict were significantly heavier at eclosion and were more susceptible to mate‐harm in terms of progeny production under continuous exposure to the males. However, these females produced more progeny upon single mating and had significantly higher longevity in absence of any male exposure—a potential evidence of trade‐offs between resistance‐related traits and other life‐history traits, such as fecundity and longevity. We also report tentative evidence, suggesting an increased male cost of interacting with more resistant females.     

Effects of energetic reserves on behavioral patterns of Mediterranean fruit flies (Diptera: Tephritidae)

The objective of this study was to associate levels of nutritional reserves (specifically lipids, sugars, and glycogen) in individual Mediterranean fruit flies, Ceratitis capitata (Diptera: Tephritidae), with observed patterns of behavior in the field. We collected females (n=255) and males (n=181) from the field, recording the time of collection and the activity they were engaged in when collected. Subsequently, we employed colorimetric biochemical techniques to determine the precise amounts of lipids, sugars, and glycogen in each individual. Lipid and sugar levels in males varied significantly according to the time of collection and the type of activity. Lipid and sugar levels in females did not vary in this manner. Sugar levels in both males and females were highest during the evening, when most feeding occurs. Males that engaged in sexual signaling in leks during the mid-afternoon had relatively low sugar and high lipid levels. Males engaged in the alternative mating tactic of fruit guarding had relatively high sugar and low lipid contents. Glycogen levels in males were high in the mornings, and a decline in glycogen content was associated with participation in leks; however, female glycogen levels did not vary significantly with time of day or activity. Our results provide quantitative evidence for the role nutrient reserves play in driving patterns of male reproductive behavior, yet suggest that factors other than sugar and lipid reserves constrain female behavior. Received: 8 April 1997 / Accepted: 23 June 1997     

Female Gryllus vocalis Field Crickets Gain Diminishing Returns from Increasing Numbers of Matings

Although female insects generally gain reproductive benefits from mating frequently, females do not mate unlimited numbers of times. This study asks whether the limit on female mating rate is imposed by trade‐offs between reproduction and survival. Female Gryllus vocalis were given the opportunity to mate 5, 10, or 15 times with novel males, and the effects on daily fecundity (egg production), fertility (proportion of eggs that were fertilized), and female post‐experimental longevity were measured. Females that mated 10 times laid more eggs and had a higher proportion of fertile eggs than females that mated 5 times. However, females that mated 15 times did not lay significantly more eggs or have a higher proportion of fertile eggs than females that mated 10 times. Although number of matings did not affect the date that females laid their last egg, mating more times was associated with a prolonged period of laying fertile eggs. Number of matings did not affect female post‐experimental longevity. Thus, there was no trade‐off between female reproductive effort and survival, even when females mated very large numbers of times. When females were allowed to mate ad libitum, the average number of times that females mated was greater than the number of times that confers maximal fitness. The lack of cost to mating explains why females might be willing to mate beyond the point of diminishing reproductive returns.