Lifetime Fitness Research Articles

The Effects of Larval Nutrition on Reproductive Performance in a Food-Limited Adult Environment

It is often assumed that larval food stress reduces lifetime fitness regardless of the conditions subsequently faced by adults. However, according to the environment-matching hypothesis, a plastic developmental response to poor nutrition results in an adult phenotype that is better adapted to restricted food conditions than one having developed in high food conditions. Such a strategy might evolve when current conditions are a reliable predictor of future conditions. To test this hypothesis, we assessed the effects of larval food conditions (low, improving and high food) on reproductive fitness in both low and high food adults environments. Contrary to this hypothesis, we found no evidence that food restriction in larval ladybird beetles produced adults that were better suited to continuing food stress. In fact, reproductive rate was invariably lower in females that were reared at low food, regardless of whether adults were well fed or food stressed. Juveniles that encountered improving conditions during the larval stage compensated for delayed growth by accelerating subsequent growth, and thus showed no evidence of a reduced reproductive rate. However, these same individuals lost more mass during the period of starvation in adults, which indicates that accelerated growth results in an increased risk of starvation during subsequent periods of food stress.

Indirect genetics effects and evolutionary constraint: an analysis of social dominance in red deer, Cervus elaphus

By determining access to limited resources, social dominance is often an important determinant of fitness. Thus, if heritable, standard theory predicts mean dominance should evolve. However, dominance is usually inferred from the tendency to win contests, and given one winner and one loser in any dyadic contest, the mean proportion won will always equal 0.5. Here, we argue that the apparent conflict between quantitative genetic theory and common sense is resolved by recognition of indirect genetic effects (IGEs). We estimate selection on, and genetic (co)variance structures for, social dominance, in a wild population of red deer Cervus elaphus, on the Scottish island of Rum. While dominance is heritable and positively correlated with lifetime fitness, contest outcomes depend as much on the genes carried by an opponent as on the genotype of a focal individual. We show how this dependency imposes an absolute evolutionary constraint on the phenotypic mean, thus reconciling theoretical predictions with common sense. More generally, we argue that IGEs likely provide a widespread but poorly recognized source of evolutionary constraint for traits influenced by competition.

Corticosterone, brood size, and hatch order in free-living Florida scrub-jay ( Aphelocoma coerulescens) nestlings

It is well known that variation in developmental conditions can have profound effects upon lifetime fitness. In altricial avian species, nestlings undergo a substantial portion of development in the nest after hatching, often in the presence of nest-mates. This can result in the formation of brood hierarchies based on age, size, and competitive ability. Measurement of baseline corticosterone (CORT) levels in developing birds may provide a means to assess whether individuals within a brood experience stress due to sibling competition or nutritional state. However, few studies have attempted to correlate corticosterone concentrations with brood hierarchies in free-living, developing birds. We investigated the degree to which corticosterone levels in nestling Florida scrub-jays ( Aphelocoma coerulescens) were predicted by brood size, hatching order, and body mass. Nestling corticosterone levels were inversely correlated with body mass but did not differ among brood sizes. Within broods of two, second-hatched nestlings had lower CORT than first-hatched nestlings, although there was no effect of hatch order in broods of three or four nestlings. The results of this study suggest that conditions within the nest, particularly those associated with within-brood hierarchies, are manifested through differential body condition and nestling corticosterone secretion. The consequences of this variation in nestling corticosterone are unknown, but development of the adult phenotype, as well as life-long survival, may be impacted.

Causes of lifetime fitness of Darwin's finches in a fluctuating environment

The genetic basis of variation in fitness of many organisms has been studied in the laboratory, but relatively little is known of fitness variation in natural environments or its causes. Lifetime fitness (recruitment) may be determined solely by producing many offspring, modified by stochastic effects on their subsequent survival up to the point of breeding, or by an additional contribution made by the high quality of the offspring owing to nonrandom mate choice. To investigate the determinants of lifetime fitness, we measured offspring production, longevity, and lifetime number of mates in four cohorts of two long-lived species of socially monogamous Darwin's finch species, Geospiza fortis and G. scandens, on the equatorial Galápagos Island of Daphne Major. Regression analysis showed that the lifetime production of fledglings was predicted by lifetime number of clutches and that recruitment was predicted by lifetime number of fledglings and longevity. There was little support for a hypothesis of selective mating by females. The offspring sired by extrapair mates were no more fit in terms of recruitment than were half-sibs sired by social mates. These findings provide insight into the evolution of life history strategies of tropical birds. Darwin's finches deviate from the standard tropical pattern of a slow pace of life by combining tropical (long lifespan) and temperate (large clutch size) characteristics. Our study of fitness shows why this is so in terms of selective pressures (fledgling production and adult longevity) and ecological opportunities (pulsed food supply and relatively low predation).

Clinal Variation in Flowering Time and Vernalisation Requirement across a 3000-M Altitudinal Range in Perennial Arabidopsis kamchatica Ssp.Kamchatica and Annual Lowland Subspecies Kawasakiana

Clines in ecologically important traits across environmental gradients provide evidence of historical natural selection. Among the many adaptive traits that are relevant in natural habitats, flowering timing is a primary determinant of a plant’s lifetime fitness. In a laboratory experiment, we studied the divergence in flowering time and vernalisation requirement among 38 populations of two Arabidopsis subspecies: perennial A. kamchatica ssp. kamchatica across an altitudinal gradient from 30 to nearly 3000 m in the Japanese Alps, and its annual lowland subspecies, kawasakiana. Flowering time with vernalisation was not different and flowering time without vernalisation was slightly different between the subspecies; however, the altitude of the source populations was the dominant determinant of the variation in these traits for the species as a whole. The flowering time increased linearly and the effect of vernalisation to shorten the flowering time increased non-linearly with increasing altitude of the source population. Low-altitude populations of ssp. kamchatica from laboratory-collected seeds showed a stronger response to vernalisation than field-collected seeds, suggesting an effect of the maternal environment. By replicating the altitudinal gradient and explicitly accounting for the maternal effect, our results clearly suggest the existence of genetically based clinal patterns that provide signs of adaptive evolution. Early flowering is probably advantageous to completing reproduction before the hot summer at low altitudes. In ssp. kamchatica, which is perennial and can reproduce even if it does not flower in its first year, the strong vernalisation requirement may delay the first reproduction at high altitudes, where the growing season is short.

Renesting of Common Terns Sterna hirundo in the life history perspective

Replacement clutches may increase the annual reproductive output of individuals and the population, but cause additional effort and may have fitness consequences. Whether longevity and lifetime reproductive success are affected by renesting is unknown. In an individual-based long-term study (1992–2009) we investigated Common Terns Sterna hirundo breeding at the colony site “Banter See” on the German North Sea coast and marked with transponders. This approach allowed us to study short-term as well as long-term consequences of relaying for both the population and individuals. In 5 of 7 years characterized by higher relaying activity, breeding success of replacement clutches was similar or even higher than that of first clutches, but in the total study period only 4.5% of all fledglings (4.4% of natal recruits) stemmed from replacement clutches. Demographic effects of relaying were minor. In most years, relaying birds were able to increase their annual reproductive output through the replacement clutch. Relaying Common Terns were high quality individuals, arriving and laying earlier, and characterized by higher age and body condition than non-relaying conspecifics. Relaying probability decreased with delayed arrival and laying date of first clutch. Survival to the next year did not differ between breeders with or without a replacement clutch. In the lifetime perspective, individuals with at least one renesting event had higher survival, longevity, lifetime reproductive success and fitness compared to birds without a replacement clutch. The higher lifetime reproductive success of the renesting individuals was achieved by a longer lifespan as well as by the reproductive output due to relaying. The positive links between survival, additional effort for replacement clutches and their success are obviously due to the fact that only those individuals relay that can cope with the additional effort required for production and care of the replacement clutch. In this way, renesting is an indicator of high individual quality and a benefit for fitness.

Direct fitness benefits of delayed dispersal in the cooperatively breeding red wolf (Canis rufus)

The existence of cooperative breeding in diverse animal taxa has inspired much interest in what nonbreeding helpers gain from participation in rearing nondescendent young. A major theoretical explanation for this phenomenon has revolved around the notion of inclusive fitness, where delayed dispersers in a family-based group gain indirect fitness benefits by fostering the viability of close relatives. There is potential, however, for direct fitness benefits in delayed dispersal itself. We explored the relationship between delayed dispersal and lifetime fitness in a reintroduced population of the cooperatively breeding red wolf, Canis rufus, which exhibits delayed dispersal but few opportunities to breed in the natal pack. We present evidence that male wolves that delayed dispersal to later ages had lower mortality risk from natural and anthropogenic sources combined and increased probability of becoming reproductive in their lifetimes. Furthermore, delayed dispersal did not result in delayed age at first reproduction. For females, however, the relative costs and benefits of delaying dispersal to later ages were more complex. In general, we provide evidence that there are direct fitness benefits to delaying dispersal in red wolves even in the absence of reproductive opportunities in the natal pack. Thus, we lend support to the hypothesis that direct fitness benefits may in themselves be sufficient to facilitate the evolution of delayed dispersal requisite to cooperatively breeding social systems. Key words: age at first dispersal, age at first reproduction, canids, cooperative breeding, lifetime reproductive probability, lifetime reproductive success, survival. [Behav Ecol]

Why do men seek status? Fitness payoffs to dominance and prestige

In many human societies, high male social status associates with higher fertility, but the means by which status increases lifetime fitness have not been systematically investigated. We analyse the pathways by which male status begets reproductive success in a small-scale, Amerindian society. Men who are more likely to win a dyadic physical confrontation, i.e. dominant men, have higher intra-marital fertility for their age, and men with more community-wide influence, i.e. prestigious men, exhibit both higher intra-marital fertility and lower offspring mortality. Both forms of status elicit support from allies and deference from competitors, but high status men are not provisioned more than their peers. Prestigious but not dominant men marry wives who first give birth at earlier ages, which multivariate analysis suggests is the strongest pathway between status and fitness in this population. Furthermore, men are motivated to pursue status because of fitness gains both within and outside of marital unions: dominant and prestigious men have more in-pair surviving offspring as well as more extra-marital affairs.

A 4D natural selection model illuminates the enigma of altruism in the Shedao pit viper

Endemic to a small island off the coast of China, the Shedao pit viper, Gloydius shedaoensis, is known for its ‘accidental altruism.’ Juvenile pit vipers often kill passerine birds too large to swallow. Large prey carcasses are scavenged by neighboring adults. In turn, adult pit vipers kill hawks that prey on juvenile pit-vipers, but are not a threat to the adults themselves. Using agent-based computer simulations, we quantified the lifetime fitness of pit viper breeders with one of three genotypes: selfish, altruistic or both selfish and altruistic. Our simulation was based on a four-dimensional (4D) model of social behavior which included interactions of pit viper offspring with predators and prey as well as conspecifics. Results showed that, over ten breeding seasons, pit viper breeders with flexible altruistic and selfish genotypes averaged seven times the number of surviving offspring relative to breeders with pure-selfish genotypes, and 23 times the number of surviving offspring as breeders with pure-altruistic genotypes. In summary, viewing animal behavior through the lens of the 4D model will extend our understanding of the evolutionary pathway to social behaviors through natural selection processes.

Rank-Related Fitness Differences and Their Demographic Pathways in Semi-Free-Ranging Rhesus Macaques (Macaca mulatta)

Researchers have explored the fitness consequences of female dominance hierarchies in many primate populations, with most studies highlighting differences in age of maturation, fertility, and offspring survival. We use resampling techniques and van Tienderen’s (2000) elasticity path analysis to identify rank-related differences in finite rate of increase (λ) and their demographic correlates among segments of a semi-free-ranging rhesus macaque population. Higher-ranking population segments grew at greater rates for some portions of the 40-yr study period. The female members of these segments achieved these lifetime fitness differences through higher fertility and especially higher adult survival rates. This is the first clear evidence that social rank influences female primate adult survival, and is a crucial fitness component for any long-lived, slow-reproducing animal. Traditional methods of comparing lifespans, and other life history variables, among rank categories fail to identify most of the rank-related differences primarily because they require completed life histories that are available only on a small number of the females known in the population.

Delayed emission of cold positronium from mesoporous materials

It is well known that ortho-positronium (ortho-Ps) atoms are emitted with high efficiency from various porous materials following the implantation of positrons. Since the ortho-Ps lifetime in a mesoporous material may be a substantial fraction of the ortho-Ps vacuum lifetime ($142$ ns), the time dependence of Ps emission may have to be considered when conducting certain types of experiments, such as time of flight measurements or pulsed ortho-Ps-laser interactions, when using this kind of target as a positronium source. By taking into account the positron implantation profile and subsequent Ps diffusion and decay in a mesoporous film we calculate the time dependent ortho-Ps emission rate $\ensuremath{\Gamma}$($t$), which in turn allows us to establish the total annihilation rate, arising from the decay of ortho-Ps both inside and outside the sample. Using time-delayed laser spectroscopy and single-shot lifetime measurements we have directly probed the rate at which Ps is emitted into vacuum from a target with $~$3-nm diameter pores and have observed delayed ortho-Ps emission that is consistent with our model. From the ortho-Ps decay spectrum we find that, whereas a simple two-component lifetime fit gives a short lifetime of $25.3$$\ifmmode\pm\else\textpm\fi{}$$0.3$ ns, an analysis that properly takes into account the emission rate yields an ortho-Ps lifetime inside the porous material of $32.3$$\ifmmode\pm\else\textpm\fi{}$$1.2$ ns, demonstrating that the ortho-Ps escape rate into vacuum can significantly modify the apparent lifetime of ortho-Ps inside a mesoporous material. Our measurements yield a Ps diffusion coefficient $D$ $=$ $0.07$ $\ifmmode\pm\else\textpm\fi{}$ $0.01$ cm${}^{2}$ ${\mathrm{s}}^{\ensuremath{-}1}$, which is consistent with a tunneling limited diffusion process.

Helper effects on pup lifetime fitness in the cooperatively breeding red wolf (Canis rufus).

The evolutionary maintenance of cooperative breeding systems is thought to be a function of relative costs and benefits to breeders, helpers and juveniles. Beneficial effects of helpers on early-life survivorship and performance have been established in several species, but lifetime fitness benefits and/or costs of being helped remain unclear, particularly for long-lived species. We tested for effects of helpers on early- and late-life traits in a population of reintroduced red wolves (Canis rufus), while controlling for ecological variables such as home-range size and population density. We found that the presence of helpers in family groups was positively correlated with pup mass and survival at low population density, but negatively correlated with mass/size at high density, with no relation to survival. Interestingly, mass/size differences persisted into adulthood for both sexes. While the presence of helpers did not advance age at first reproduction for pups of either sex, females appeared to garner long-term fitness benefits from helpers through later age at last reproduction, longer reproductive lifespan and a greater number of lifetime reproductive events, which translated to higher lifetime reproductive success. In contrast, males with helpers exhibited diminished lifetime reproductive performance. Our findings suggest that while helper presence may have beneficial short-term effects in some ecological contexts, it may also incur long-term sex-dependent costs with critical ramifications for lifetime fitness.

Synergy of multiple partners, including freeloaders, increases host fitness in a multispecies mutualism

Understanding cooperation is a central challenge in biology, because natural selection should favor "free-loaders" that reap benefits without reciprocating. For interspecific cooperation (mutualism), most approaches to this paradox focus on costs and benefits of individual partners and the strategies mutualists use to associate with beneficial partners. However, natural selection acts on lifetime fitness, and most mutualists, particularly longer-lived species interacting with shorter-lived partners (e.g., corals and zooxanthellae, tropical trees and mycorrhizae) interact with multiple partner species throughout ontogeny. Determining how multiple partnerships might interactively affect lifetime fitness is a crucial unexplored link in understanding the evolution and maintenance of cooperation. The tropical tree Acacia drepanolobium associates with four symbiotic ant species whose short-term individual effects range from mutualistic to parasitic. Using a long-term dataset, we show that tree fitness is enhanced by partnering sequentially with sets of different ant symbionts over the ontogeny of a tree. These sets include a "sterilization parasite" that prevents reproduction and another that reduces tree survivorship. Trees associating with partner sets that include these "parasites" enhance lifetime fitness by trading off survivorship and fecundity at different life stages. Our results demonstrate the importance of evaluating mutualism within a community context and suggest that lifespan inequalities among mutualists may help cooperation persist in the face of exploitation.

Mixed-Mating Strategies and their Sensitivity to Abiotic Variation in Viola Lanceolata L. (Violaceae)~!2010-04-09~!2010-06-08~!2010-09-15~!

Mating-system expression is sensitive to environmental conditions, and can be an important determinant of lifetime fitness because progeny that are produced via outcrossing vs. selfing may differ in quality. We quantified sexual and asexual reproduction in Viola lanceolata, a regionally threatened species, across populations that varied in disturbance history and across microsites that differed in percent soil moisture, irradiance, and temperature. In V. lanceolata, reproduction can occur sexually through facultatively outcrossing chasmogamous (CH) flowers and obligately selfing cleistogamous (CL) flowers in addition to asexually via stolons. The frequency of individuals producing CH and CL flowers differed among sites as did the frequency of vegetative reproduction. Interestingly, sites also differed in fruit maturation success, with ~33, 100, and 16% of the CH fruits matured in the oldest, intermediate, and most-recently disturbed populations respectively. Analogous site differences in CL fruit maturation were observed. Cleistagamous, but not CH, reproduction was also dependent on percent soil moisture. The observed differences in fruit maturation success likely lead to variable rates of outcrossed vs. self-fertilized seed production; as a consequence, populations are likely to differ in genetic structure and in relative dependence on chasmogamy vs. cleiostogamy for population growth. Finally, CL flower and stolon production were negatively correlated, suggesting a tradeoff between sexual and asexual reproduction that might affect population growth.

INFERRING FITNESS LANDSCAPES

Since 1983, study of natural selection has relied heavily on multiple regression of fitness on the values for a set of traits via ordinary least squares (OLSs), as proposed by Lande and Arnold, to obtain an estimate of the quadratic relationship between fitness and the traits, the fitness surface. However, well-known statistical problems with this approach can affect inferences about selection. One key concern is that measures of lifetime fitness do not conform to a normal or any other standard sampling distribution, as needed to justify the usual statistical tests. Another is that OLS may yield an estimate of the sign of the fitness function's curvature that is opposite to the truth. We here show that the recently developed aster modeling approach, which explicitly models the components of fitness as the basis for inferences about lifetime fitness, eliminates these problems. We illustrate selection analysis via aster using simulated datasets involving five fitness components expressed in each of four years. We demonstrate that aster analysis yields accurate estimates of the fitness function in cases in which OLS misleads, as well as accurate confidence regions for directional selection gradients. Further, to evaluate selection when many traits are under consideration, we recommend model selection by information criteria and frequentist model averaging.

Trait‐mediated interactions and lifetime fitness of the invasive plant Centaurea solstitialis

Plants interact with numerous enemies and mutualists simultaneously and sequentially. Such multispecies interactions can give rise to trait-mediated indirect effects that are likely to be common in nature but which are also inherently difficult to predict. Understanding multispecies interactions is also important in the use of biological control agents to control invasive plants because modern approaches to biocontrol rely on releasing multiple agents for each target weed. Centaurea solstitialis is one of the most problematic invasive weeds in California, USA, and the weevil Eustenopus villosus is its dominant biological control agent. We conducted a field experiment to quantitatively assess the direct effect of the recently approved biocontrol pathogen Puccinia jaceae f.s. solstitialis on plant performance and any indirect effects that might arise by altering the plant's interactions with Eustenopus or its pollinators (principally the nonnative Apis mellifera). We documented both synergy and interference between the two biocontrol agents depending on the life stage of the weevil. Puccinia infection increased the impact of bud-feeding by the adult weevils but reduced the impact of seed-feeding by larval weevils. Neither infection nor Eustenopus attack had an effect on pollinator visitation. The net effect was that attack by both the pathogen and the weevil did not reduce plant fitness relative to plants attacked only by the weevil. Because the consequence to the plant of interacting with one species may depend on the presence or absence of other interacting species, a careful consideration of multispecies interactions may be necessary for the selection of biocontrol agents that act in a complementary manner to reduce plant fitness. Likewise, relatively tractable weed-biocontrol systems allow us to examine multispecies interactions that can be difficult to study experimentally in native systems that are composed of numerous species with well-established populations.

Phenotypic plasticity and fitness in egg parasitoids

Several proxies can be used to estimate the fitness of egg parasitoids: size, longevity, fecundity, mating ability and vagility. All these proxies are positively correlated with the lifetime fitness gain of an individual. However, the phenotypic plasticity, which is the ability of a genotype to produce distinct phenotypes depending on environmental conditions, may alter the value of these proxies. Host related factors (host species and quality), competition and duration of development will influence the proxies expressed by a given phenotype. When the phenotype is modified by the temperature at which an individual develops, the resulting phenotype will vary based on the life history strategy of the parasitoid. While in koinobiont species an increase in size is positively correlated with longevity and fecundity, the reverse occurs with idiobiont parasitoids. Using size as a proxy could thus be misleading depending on the factors that influence the size of the adult.

Carry-over effects of the larval environment on post-metamorphic performance in two hylid frogs

Life history theory and empirical studies suggest that large size or earlier metamorphosis are suitable proxies for increased lifetime fitness. Thus, across a gradient of larval habitat quality, individuals with similar phenotypes for these traits should exhibit similar post-metamorphic performance. Here we examine this paradigm by testing for differences in post-metamorphic growth and survival independent of metamorphic size in a temperate (spring peeper, Pseudacris crucifer) and tropical (red-eyed treefrog, Agalychnis callidryas) anuran reared under differing larval conditions. For spring peepers, increased food in the larval environment increased post-metamorphic growth efficiency more than predicted by metamorphic phenotype and led to increased mass. Similarly, red-eyed treefrogs reared at low larval density ended the experiment at a higher mass than predicted by metamorphic phenotype. These results show that larval environments can have delayed effects not captured by examining only metamorphic phenotype. These delayed effects for the larval environment link larval and juvenile life history stages and could be important in the population dynamics of organisms with complex life cycles.

Strong and Consistent Social Bonds Enhance the Longevity of Female Baboons

Longevity is a major component of variation in fitness in long-lived iteroparous species [1-4]. Among female baboons, variation in breeding lifespan accounts for approximately 50% of the variation in lifetime fitness [5, 6]. However, we know little about the causes of variation in longevity in primates or other long-lived mammals. Savannah baboons form strong, equitable, and enduring relationships with specific female partners, particularly with close relatives and agemates [7-10]. The quality of females' social relationships influences their ability to cope with stressful events [11-13] and is associated with variation in female reproductive success [9, 14]. Here we show that dominance rank and the quality of close social bonds have independent effects on the longevity of female chacma baboons (Papio hamadryas ursinus). High-ranking females live longer than lower-ranking females. In addition, females who form stronger and more stable social bonds with other females live significantly longer than females who form weaker and less stable relationships. These data extend our understanding of the adaptive value of social bonds in baboons and complement a growing body of evidence that indicates that social bonds have adaptive value in a range of taxa, from mice to humans [9, 14-19].

Fitness-Associated Sexual Reproduction in a Filamentous Fungus

Sex is a long-standing evolutionary enigma. Although the majority of eukaryotes reproduce sexually at least sometimes [1-3], the evolution of sex from an asexual ancestor has been difficult to explain because it requires sexually reproducing lineages to overcome the manifold costs of sex, including the destruction of favorable gene combinations created by selection [4, 5]. Conditions for the evolution of sex are much broader if individuals can reproduce either sexually or asexually (i.e., facultative sex) and allocate disproportionately more resources to sex when their fitness is low (fitness-associated-sex or FAS [6-10]). Although facultatively sexual organisms have been shown to engage in more sex when stressed [11], direct evidence for FAS is lacking. We provide evidence using 53 genotypes of the filamentous fungus Aspergillus nidulans in a reciprocal transplant experiment across three environments. Different genotypes achieved highest fitness in different environments and genotypes invested relatively more in sex in environments in which their fitness was lower, showing that allocation to sexual reproduction is a function of how well-adapted a genotype is to its environment. FAS in A. nidulans is unlikely to have evolved as a strategy to resist or avoid stress because asexual spores are more dispersive and equally resistant [12, 13].