Climate‐dependent costs of reproduction: Survival and fecundity costs decline with length of the growing season and summer temperature

Costs of reproduction are expected to vary with environmental conditions thus influencing selection on life‐history traits. Yet, the effects of habitat conditions and climate on trade‐offs among fitness components remain poorly understood. For 2–5 years, we quantified costs of experimentally increased reproduction in two populations (coastal long‐season vs. inland short‐season) of two long‐lived orchids that differ in natural reproductive effort (RE; 30 vs. 75% fruit set). In both species, survival costs were found only at the short‐season site, whereas growth and fecundity costs were evident at both sites, and both survival and fecundity costs declined with increasing growing season length and/or summer temperature. The results suggest that the expression of costs of reproduction depend on the local climate, and that climate warming could result in selection favouring increased RE in both study species.     

Early reproductive investment,senescence and lifetime reproductive success in female Asian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early‐life over late‐life reproduction. Studies on natural vertebrate populations show early reproduction may impair later‐life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early‐life reproduction and female age‐specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age‐specific fecundity and offspring survival, but significantly impaired a female's own later‐life survival. Despite the negative effects of early reproduction on late‐life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade‐off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later‐life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi‐)captive breeding programmes of this endangered species.     

Size delays female senescence in a medium sized marsupial: The effects of maternal traits on annual fecundity in the northern brown bandicoot (Isoodon macrourus)

The degree to which females allocate resources between current reproduction, future fecundity and survival is a central theme in life history theory. We investigated two hypotheses proposed to explain patterns of reproductive investment, terminal investment and senescence, by examining the effects of maternal traits (age and maternal mass) on annual fecundity in female northern brown bandicoots, Isoodon macrourus (Marsupialia: Peramelidae). We found that annual fecundity in females declined in their final year of reproduction, indicating reproductive senescence. Maternal mass significantly influenced the rate of senescence and, in turn, a female's lifetime reproductive output. Mass had little effect on fecundity in 1st and 2nd year females, but a positive relationship with fecundity in 3rd year females. This meant that heavy, 3rd year females did not suffer the decline in fecundity shown in light 3rd year females. For 1st year females, mass and leg length increased between their first and second reproductive seasons, indicating a temporary shift, from the allocation of resources to reproduction, to increasing condition or structural size post their first breeding event. There were no net changes to body mass in subsequent years. We suggest that this year of post‐reproductive growth has important consequences for senescent effects on reproduction. Overall, results provided support for the effects of senescence on annual fecundity. Our findings were not consistent with the terminal investment hypothesis; reproductive output did not increase in females' final reproductive season despite a rapid decline in survival. However, this notion cannot be entirely dismissed; other measures of reproductive performance not examined here (e.g. offspring mass) may have provided an indication that females did increase their effort at the end of their lifespan. This study highlights the difficulty of measuring reproductive costs and the importance of understanding the combined effects of specific characteristics of an individual when interpreting reproductive strategies in iteroparous organisms.     

Twelve fundamental life histories evolving through allocation‐dependent fecundity and survival

An organism's life history is closely interlinked with its allocation of energy between growth and reproduction at different life stages. Theoretical models have established that diminishing returns from reproductive investment promote strategies with simultaneous investment into growth and reproduction (indeterminate growth) over strategies with distinct phases of growth and reproduction (determinate growth). We extend this traditional, binary classification by showing that allocation‐dependent fecundity and mortality rates allow for a large diversity of optimal allocation schedules. By analyzing a model of organisms that allocate energy between growth and reproduction, we find twelve types of optimal allocation schedules, differing qualitatively in how reproductive allocation increases with body mass. These twelve optimal allocation schedules include types with different combinations of continuous and discontinuous increase in reproduction allocation, in which phases of continuous increase can be decelerating or accelerating. We furthermore investigate how this variation influences growth curves and the expected maximum life span and body size. Our study thus reveals new links between eco‐physiological constraints and life‐history evolution and underscores how allocation‐dependent fitness components may underlie biological diversity.     

THE EVOLUTION OF REPRODUCTIVE EFFORT IN SQUAMATE REPTILES: COSTS,TRADE-OFFS,AND ASSUMPTIONS RECONSIDERED

We evaluated Shine and Schwarzkopf's (SS) model of the evolution of reproductive effort (RE) in squamate reptiles. They suggested that fecundity trade-offs were unimportant in the evolution of RE in most squamate reptiles and that only survival trade-offs needed to be considered. However, we show that by assuming no variation in offspring size exists, and that adult mortality is episodic, the results of the SS model are not general. By extension, we argue that conclusions drawn about factors important in the evolution of RE in squamate reptiles are premature. Using a modified version of the SS model, we demonstrate that variation in the form of trade-offs relating offspring size and survival substantially affect relationships among clutch size, relative clutch mass, and lifetime reproductive success. We also demonstrate that the way in which adult mortality is simulated drastically affects conclusions about the potential fecundity trade-offs experienced by populations of squamate reptiles. Finally, we suggest that a complete understanding of the evolution of RE will come from theory that incorporates trade-offs between offspring size and quality, as well as other system-specific constraints on the allocation of energy to growth, maintenance, storage, and reproduction.     

Reproductive effort in viscous populations

Abstract.— Here I study a kin selection model of reproductive effort, the allocation of resources to fecundity versus survival, in a patch-structured population. Breeding females remain in the same patch for life. Offspring have costly, partial long-distance dispersal and compete for breeding sites, which become vacant upon the death of previous occupants. The main result is that the evolutionarily stable reproductive effort decreases as offspring dispersal rate increases. The result can be understood as follows: In a well-mixed population with global competition, neither adults nor juveniles compete with relatives, but in a patch-structured population with dispersal restricted to the juvenile phase, juveniles experience relatively less competition with relatives than adults, thus making juveniles relatively more valuable. Because this asymmetry between adults and juveniles decreases with the dispersal rate, so does the evolutionarily stable level of allocation to fecundity.     

Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis

Body size can influence an organism's microevolutionary fitness either via ecological factors (ecological selection) or changes in reproductive output (sexual or fecundity selection). Published studies on sexual dimorphism in reptiles have generally focussed on sexual-selective forces on males, under the implicit assumption that the intensity of fecundity selection in females (and hence, overall selection on female body size) is likely to be relatively consistent among lineages. In this paper, we explore the degree to which larger body size enhances ecological attributes (e.g., food intake, growth, survival) and reproductive output (reproductive frequency, litter size, offspring size, offspring viability) in free-ranging female aspic vipers, Vipera aspis . The less-than-annual reproductive frequency of these animals allows us to make a direct comparison between females in years during which they concentrate on "ecological" challenges (especially building energy reserves) versus reproductive challenges (producing a litter). Because female snakes have limited abdominal space to hold the clutch (litter), we expect that fecundity should depend on body size. However, our data show that larger body size had a more consistent effect on ecological attributes (such as feeding rates and "costs of reproduction") than on reproductive output per se. Indeed, total reproductive output was maximised at intermediate body sizes. These results suggest that variation in female body size among and within species (and hence, in the degree of sexual dimorphism) may be driven by the ecological as well as reproductive consequences of body size variation in both sexes.     

Environmental heterogeneity generates fluctuating selection on a secondary sexual trait

In any population in which resources are limiting, the allocation of resources toward increased reproductive success may generate costs to survival [1-8]. The relationship between a sexually selected trait and fitness will therefore represent a balance between its relative associations with fecundity versus viability [3, 6, 7]. Because the risk of mortality in a population is likely to be heavily determined by ecological conditions, survival costs may vary as a function of the prevailing environment [7]. As a result, for populations experiencing heterogeneous ecological conditions, there may not be a single optimal level of allocation toward reproduction versus survival [9]. Here, we show that early viability and fecundity selection act in opposing directions on a secondary sexual trait and that their relative magnitude depends upon ecological conditions, generating fluctuating selection. In a wild population of Soay sheep (Ovis aries), phenotypic and genetic associations between male horn growth and lifetime reproductive success were positive under good environmental conditions (because of increased breeding success) and negative under poor environmental conditions (because of reduced survival). In an unpredictable environment, high allocation to early horn growth is a gamble that will only pay off if ensuing conditions are favorable. Such fluctuating selection may play an important role in preventing the erosion of genetic variance in secondary sexual traits.     

Energy versus risk: costs of reproduction in free‐ranging pythons in tropical Australia

Abstract Data from a 12‐year field study have allowed us to quantify ‘costs of reproduction’ in a natural population of water pythons (Liasis fuscus) in tropical Australia. Both sexes of pythons cease feeding during the reproductive season. For males, this involves fasting for a 6 week period. Adult males lose weight rapidly over this period (approximately 17% of their body mass) but regain condition in the following months, and do not experience reduced survival. In contrast, reproductive adult females cease feeding for 3 months, lose an average of 44% of their body mass over this period, and experience increased mortality. A causal link between reproductive output and reduced female survival is supported by (i) a decrease in survival rates at female maturation; (ii) a correlation between survival rates and frequency of reproduction, in a comparison among different size classes of adult pythons; and (iii) a lowered survival rate for females that allocated more energy to reproduction. Hence, both sexes experience substantial energy costs of reproduction, but a relatively higher energy cost translates into a survival cost only in females. Such non‐linearities in the relationship between energy costs and survival costs may be widespread, and challenge the value of simple energy‐based measures of 'reproductive effort’.     

Survival costs of reproduction predict age-dependent variation in maternal investment

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.     

SEXUAL SIZE DIMORPHISM AND SELECTION IN THE WILD IN THE WATERSTRIDER AQUARIUS REMIGIS: LIFETIME FECUNDITY SELECTION ON FEMALE TOTAL LENGTH AND ITS COMPONENTS

Darwin's fecundity advantage model is often cited as the cause of female biased size dimorphism, however, the empirical studies of lifetime selection on male and female body size that would be required to demonstrate this are few. As a component of a study relating sexual size dimorphism to lifetime selection in natural populations of the female size-biased waterstrider Aquarius remigis (Hemiptera: Gerridae), we estimated coefficients for daily fecundity selection, longevity selection, and lifetime fecundity selection acting on female body size and components of body size for two consecutive generations. Daily fecundity was estimated using females confined in field enclosures and reproductive survival was estimated by twice-weekly recaptures. We found that daily fecundity selection favored females with longer total length through direct selection acting on abdomen length. Longevity selection favored females with smaller total length. When daily fecundity and reproductive longevity were combined to estimate lifetime fecundity we found significant balancing selection acting on total length in both years. The relationship between daily fecundity and reproductive longevity also reveals a significant cost of reproduction in one of two years. We relate these selection estimates to previous estimates of sexual selection on male body size and consider the relationship between contemporary selection and sexual size dimorphism.     

Herbivore-mediated ecological costs of reproduction shape the life history of an iteroparous plant

Plant reproduction yields immediate fitness benefits but can be costly in terms of survival, growth, and future fecundity. Life-history theory posits that reproductive strategies are shaped by trade-offs between current and future fitness that result from these direct costs of reproduction. Plant reproduction may also incur indirect ecological costs if it increases susceptibility to herbivores. Yet ecological costs of reproduction have received little empirical attention and remain poorly integrated into life-history theory. Here, we provide evidence for herbivore-mediated ecological costs of reproduction, and we develop theory to examine how these costs influence plant life-history strategies. Field experiments with an iteroparous cactus (Opuntia imbricata) indicated that greater reproductive effort (proportion of meristems allocated to reproduction) led to greater attack by a cactus-feeding insect (Narnia pallidicornis) and that damage by this herbivore reduced reproductive success. A dynamic programming model predicted strongly divergent optimal reproductive strategies when ecological costs were included, compared with when these costs were ignored. Meristem allocation by cacti in the field matched the optimal strategy expected under ecological costs of reproduction. The results indicate that plant reproductive allocation can strongly influence the intensity of interactions with herbivores and that associated ecological costs can play an important selective role in the evolution of plant life histories.     

Sexual dimorphism explains residual variance around the survival‐reproduction tradeoff in lizards: Implications for sexual conflict over life‐history evolution*

The tradeoff between survival and reproduction is a central feature of life‐history variation, but few studies have sought to explain why females of some species exhibit relatively lower survival than expected for a given level of reproductive effort (RE). Intralocus sexual conflict theory proposes that sex differences in selection on survival and RE may, by virtue of shared genes underlying these components of fitness, prevent females from optimizing this life‐history tradeoff. To test this hypothesis, we used a phylogenetically based comparative analysis of published estimates for mean annual survival and RE from females of 82 lizard species to (1) characterize the tradeoff between survival and reproduction and (2) test whether variation around this tradeoff is explained by sexual size dimorphism (SSD), a potential proxy for sexual conflict over life‐history traits. Across species, we found a strong negative correlation between mean annual survival and RE, confirming this classic life‐history tradeoff. Although residual variance around this tradeoff is unrelated to the absolute magnitude of SSD, it is strongly related to the direction of SSD. Specifically, we found that females have lower survival than expected for a given level of RE in female‐larger species, whereas they have higher survival than expected in male‐larger species. Given that female‐larger SSD is thought to reflect selection for increased fecundity, our results suggest that intralocus sexual conflict may be particularly likely to constrain female life‐history evolution in situations where increased RE is favored, but the phenotypes that facilitate this increase (e.g., body size) are constrained by antagonistic selection on males.     

Path analysis of natural selection via survival and fecundity across contrasting environments in Avena barbata

We employed path analysis to analyse natural selection through two major fitness components in each of three contrasting environments. Using a randomized block design, 188 Recombinant Inbred Lines (RILs) derived from a cross between contrasting ecotypes of Avena barbata were planted in common gardens in the greenhouse, and in two field sites typical of each ecotype’s native habitat. Individuals were monitored for germination phenology, early growth, survival, final size, flowering phenology, reproductive allocation, fecundity and lifetime reproductive success. The variance/covariance matrix of the RIL (genotype) means was fit to a path model in which total fitness was made up of survival and fecundity (of survivors) components. In the greenhouse, all fitness variation was determined by fecundity variation (with no mortality), which was itself primarily determined by reproductive allocation mediated by date of first flowering. By contrast, in the field, early growth was the major determinant of survival, and final size was the major determinant of fecundity. Both components of fitness affected lifetime reproductive success equally in the field. Thus the major difference between greenhouse and field seems to be a shift from selection on allocation patterns in adults, to selection on resource acquisition, especially at earlier life stages. The pattern of selection was similar in the two field sites, despite the contrasting environments.     

Are reproductive and somatic senescence coupled in humans? Late, but not early, reproduction correlated with longevity in historical Sami women

Evolutionary theory of senescence emphasizes the importance of intense selection on early reproduction owing to the declining force of natural selection with age that constrains lifespan. In humans, recent studies have, however, suggested that late-life mortality might be more closely related to late rather than early reproduction, although the role of late reproduction on fitness remains unclear. We examined the association between early and late reproduction with longevity in historical post-reproductive Sami women. We also estimated the strength of natural selection on early and late reproduction using path analysis, and the effect of reproductive timing on offspring survival to adulthood and maternal risk of dying at childbirth. We found that natural selection favoured both earlier start and later cessation of reproduction, and higher total fecundity. Maternal age at childbirth was not related to offspring or maternal survival. Interestingly, females who produced their last offspring at advanced age also lived longest, while age at first reproduction and total fecundity were unrelated to female longevity. Our results thus suggest that reproductive and somatic senescence may have been coupled in these human populations, and that selection could have favoured late reproduction. We discuss alternative hypotheses for the mechanisms which might have promoted the association between late reproduction and longevity.     

The role of fecundity and reproductive effort in defining life‐history strategies of North American freshwater mussels

Selection is expected to optimize reproductive investment resulting in characteristic trade‐offs among traits such as brood size, offspring size, somatic maintenance, and lifespan; relative patterns of energy allocation to these functions are important in defining life‐history strategies. Freshwater mussels are a diverse and imperiled component of aquatic ecosystems, but little is known about their life‐history strategies, particularly patterns of fecundity and reproductive effort. Because mussels have an unusual life cycle in which larvae (glochidia) are obligate parasites on fishes, differences in host relationships are expected to influence patterns of reproductive output among species. I investigated fecundity and reproductive effort (RE) and their relationships to other life‐history traits for a taxonomically broad cross section of North American mussel diversity. Annual fecundity of North American mussel species spans nearly four orders of magnitude, ranging from < 2000 to 10 million, but most species have considerably lower fecundity than previous generalizations, which portrayed the group as having uniformly high fecundity (e.g. > 200000). Estimates of RE also were highly variable, ranging among species from 0.06 to 25.4%. Median fecundity and RE differed among phylogenetic groups, but patterns for these two traits differed in several ways. For example, the tribe Anodontini had relatively low median fecundity but had the highest RE of any group. Within and among species, body size was a strong predictor of fecundity and explained a high percentage of variation in fecundity among species. Fecundity showed little relationship to other life‐history traits including glochidial size, lifespan, brooding strategies, or host strategies. The only apparent trade‐off evident among these traits was the extraordinarily high fecundity of Leptodea, Margaritifera, and Truncilla, which may come at a cost of greatly reduced glochidial size; there was no relationship between fecundity and glochidial size for the remaining 61 species in the dataset. In contrast to fecundity, RE showed evidence of a strong trade‐off with lifespan, which was negatively related to RE. The raw number of glochidia produced may be determined primarily by physical and energetic constraints rather than selection for optimal output based on differences in host strategies or other traits. By integrating traits such as body size, glochidial size, and fecundity, RE appears more useful in defining mussel life‐history strategies. Combined with trade‐offs between other traits such as growth, lifespan, and age at maturity, differences in RE among species depict a broad continuum of divergent strategies ranging from strongly r‐selected species (e.g. tribe Anodontini and some Lampsilini) to K‐selected species (e.g. tribes Pleurobemini and Quadrulini; family Margaritiferidae). Future studies of reproductive effort in an environmental and life‐history context will be useful for understanding the explosive radiation of this group of animals in North America and will aid in the development of effective conservation strategies.     

Early-life reproduction is associated with increased mortality risk but enhanced lifetime fitness in pre-industrial humans

The physiology of reproductive senescence in women is well understood, but the drivers of variation in senescence rates are less so. Evolutionary theory predicts that early-life investment in reproduction should be favoured by selection at the cost of reduced survival and faster reproductive senescence. We tested this hypothesis using data collected from preindustrial Finnish church records. Reproductive success increased up to age 25 and was relatively stable until a decline from age 41. Women with higher early-life fecundity (ELF; producing more children before age 25) subsequently had higher mortality risk, but high ELF was not associated with accelerated senescence in annual breeding success. However, women with higher ELF experienced faster senescence in offspring survival. Despite these apparent costs, ELF was under positive selection: individuals with higher ELF had higher lifetime reproductive success. These results are consistent with previous observations in both humans and wild vertebrates that more births and earlier onset of reproduction are associated with reduced survival, and with evolutionary theory predicting trade-offs between early reproduction and later-life survival. The results are particularly significant given recent increases in maternal ages in many societies and the potential consequences for offspring health and fitness.     

Survival costs of reproduction in a short-lived perennial plant: Live hard, die young

According to life-history theory, reproductive investments involve costs in terms of growth, future fecundity, and/or survival. However, studies to date have often failed to detect costs of reproduction, with survival costs among the less documented. We investigated the cost of reproduction in Helianthemum squamatum (Cistaceae), a short-lived perennial of semiarid Mediterranean environments. After experimental flower removal, we evaluated next season's growth, reproduction, and survival of the plants. We also monitored an indicator of plant physiological status (F(v)/F(m)) and leaf nutrient concentration at key phenological stages during reproduction. Survival rate in deblossomed plants was significantly higher than in control plants. As far as we know, this is the first experimental evidence of a survival cost of reproduction in a perennial plant. In contrast, no cost to growth or reproduction was found during the next season, and no significant differences in F(v)/F(m) or leaf nutrients were found between control and deblossomed plants. Helianthemum squamatum's success in semiarid Mediterranean ecosystems seems to rely on a persistent seed bank, combined with a sustained high reproductive output at the expense of survival. We conclude that this strategy might be more common than previously thought among short-lived shrubby plants growing in stressful Mediterranean areas.     

The consequences of facultative sex in a prey adapting to predation

A species reproductive mode, along with its associated costs and benefits, can play a significant role in its evolution and survival. Facultative sexuality, being able to reproduce both sexually and asexually, has been deemed evolutionary favourable as the benefits of either mode may be fully realized. In fact, many studies have focused on identifying the benefits of sex and/or the forces selecting for increased rates of sex using facultative sexual species. The costs of either mode, however, can also have a profound impact on a population's evolutionary trajectory. Here, we used experimental evolution and fitness assays to investigate the consequences of facultative sexuality in prey adapting to predation. Specifically, we compared the adaptive response of algal prey populations exposed to constant rotifer predation and which had alternating cycles of asexual and sexual reproduction where sexual episodes were either facultative (sexual and asexual progeny simultaneously propagated) or obligate (only sexual progeny propagated). We found that prey populations with facultative sexual episodes reached a lower final relative fitness and suffered a greater trade‐off in traits under selection, that is defence and competitive ability, as compared to prey populations with obligate sexual episodes. Our results suggest that costs associated with sexual reproduction (germination time) and asexual reproduction (selection interference) were amplified in the facultative sexual prey populations, leading to a reduction in the net advantage of sexuality. Additionally, we found evidence that the cost of sex was reduced in the obligate sexual prey populations because increased selection for sex was observed via the spontaneous production of sexual cells. These results show that certain costs associated with facultative sexuality can affect an organism's evolutionary trajectory.     

Brood size manipulations within the natural range did not reveal intragenerational cost of reproduction in the Willow Tit Parus montanus

To test for the existence of a reproductive cost, we manipulated brood sizes (-2 and +2 nestlings) over 6 years in a northern population of Willow Tits Parus montanus breeding in natural holes. Possible effects were sought in subsequent survival and fecundity of the parents. Parents given extra chicks made more feeding visits than did parents with reduced and control broods. However, this was not reflected in differences in parental body-weight between groups at the end of the nestling period. Brood size manipulation did not significantly affect female or male survival. In 4 out of 6 years, there was a weak and nonsignificant effect on male survival, consistent with a cost of reproduction. Female and male fecundity in the year following the experiment was not affected by the manipulations. Thus, the data do not give evidence of an intragenerational cost of reproduction in the Willow Tit. Parents appeared unwilling to increase their breeding effort to a level which jeopardized their own survival or future breeding success. It is possible that, because of the time constraints in northern latitudes, females work under their capacity and lay smaller clutches than would otherwise be most profitable. Thus, no costs to the parents would be expected as a consequence of manipulations. These results suggest that the current reproductive rate is not maintained by reproductive cost in the Willow Tit. However, the results do not rule out the possibility that selection has operated outside the current range of reproductive rates during evolutionary history of the species.