Fitness measures in selection analyses: sensitivity to the overall number of offspring produced in a lifetime

Age at first (α) and last (ω) breeding are important life‐history traits; however, the direction and strength of selection detected on traits may vary depending on the fitness measure used. We provide the first estimates of lifetime breeding success (LBS) and λ_ind (the population growth rate of an individual) of European badgers Meles meles, by genotyping 915 individuals, sampled over 18 years, for 22 microsatellites. Males are slightly larger than females, and the opportunity for selection was slightly greater for males, as predicted. λ_ind and LBS both performed well in predicting the number of grand‐offspring, and both detected selection for a late ω, until the age of eight. Differential selection (S′_α) for an early α, however, was only detected using LBS, not with λ_ind. In declining populations (λ_ind < 1) selection favours reproduction later in life, whereas early reproduction is selected in increasing populations (λ_ind > 1). As 41% of badgers were assigned only one offspring (λ_ind < 1), whereas 40% were assigned more than two (λ_ind > 1), this cancelled out S′_α measured by λ_ind.     

Lifetime reproductive success,selection on lifespan,and multiple sexual ornaments in male European barn swallows

Natural and sexual selection arise when individual fitness varies according to focal traits. Extra‐pair paternities (EPPs) can affect the intensity of selection by influencing variance in fitness among individuals. Studies of selection require that individual fitness is estimated using proxies of lifetime reproductive success (LRS). However, estimating LRS is difficult in large, open populations where EPPs cause reallocation of biological paternity. Here, we used extensive field sampling to estimate LRS in a population of barn swallows (Hirundo rustica) to estimate selection on lifespan and ornamental traits of males. We found selection on lifespan mediated both by within‐ and extra‐pair fertilization success and selection on tail length mediated by within‐ but not extra‐pair fertilization success. In addition, we found selection on tail white spots via extra‐pair fertilization success after controlling for selection on other traits. These results were not confounded by factors that hamper studies of LRS, including nonexhaustive sampling of offspring and biased sampling of males. Hence, natural and sexual selection mediated by LRS operates on lifespan, tail length, and size of the tail white spots in barn swallows.     

Lifetime reproductive success in common buzzard, Buteo buteo: from individual variation to population demography

We studied annual and lifetime reproductive success (LRS) of both sexes of common buzzard Buteo buteo in eastern Westphalia, Germany. We followed a bottom‐up approach starting from individual breeding attempts, over lifetime reproductive success to derive population demography. Annual breeding performance and survival followed a quadratic relationship with breeding experience; individuals starting their breeding career were less likely to survive and breed successfully than birds of intermediate breeding experience. According to an analysis of selection gradients, both the opportunity and intensity of selection peaked in the early stages of the breeding career. The distribution of both LRS and another fitness measure, λ, was highly skewed, with ca 17% of adult birds producing 50% of fledglings in both sexes. Besides breeding life span and number of breeding attempts, habitat quality and plumage morph were significant predictors of LRS. There were strong differences in LRS and λ between the plumage morphs in both sexes: intermediate pigmented buzzards were much more successful than either dark or light ones. There was no significant difference between buzzard cohorts either in LRS or λ, nor did these fitness measures differ between individuals starting their breeding career at different conditions of food availability. Based on individual life histories, we formed a transition matrix and analysed its properties to study the population as a whole. This analysis showed that the population growth rate was close to unity (0.906, bootstrapped 95% confidence limits: 0.834 and 0.962). Analysis of reproductive values and elasticities further emphasised colour morph differences: the contribution of intermediate individuals to population growth greatly exceeded that of dark or light individuals. Thus most phenomena on all levels from individual breeding attempts over lifetime reproductive success to population demography can be explained by the fitness differences between the colour morphs with the intermediate morph maintaining the current population renewal potential.     

Increased lifetime reproductive success of first‐hatched siblings in Common Kestrels Falco tinnunculus

Order of birth has profound consequences on offspring across taxa during development and can have effects on individuals later in life. In birds, differential maternal allocation and investment in their progeny lead to variance in the environmental conditions that offspring experience during growth within the brood. In particular, laying and hatching order have been proposed to influence individual quality during the growing period, but little is known about the fitness consequences that these two factors have for offspring from a lifetime perspective. We explored the effect of laying and hatching order on post‐fledgling survival (measured as recruitment probability) and lifetime reproductive success (LRS) in Common Kestrels Falco tinnunculus, using a long‐term and individual‐based dataset. First‐hatched chicks showed higher survival probability and LRS than their siblings. This effect was not due to body condition of the individuals at adulthood, the quality of their mates or the reproductive outcome compared with later‐hatched individuals. Instead, first‐hatched chicks had a higher recruitment probability. This could be explained by the higher body condition attained by first‐hatched chicks at the end of the nesting period, perhaps due to an enhanced competitive advantage for food over their siblings at the time of hatching. Laying order, in contrast to hatching order, appeared to have little or no effect on LRS. Our results suggest that hatching order within siblings predicts fitness, and that better early‐life conditions during growth experienced by first‐hatched chicks improve first survival and then recruitment, resulting in an enhanced LRS.     

THE EFFECT OF MATERNAL AGE AND REPRODUCTIVE HISTORY ON OFFSPRING SURVIVAL AND LIFETIME REPRODUCTION IN PREINDUSTRIAL HUMANS

Senescence is one of the least understood aspects of organism life history. In part, this stems from the relatively late advent of complete individual‐level datasets and appropriate statistical tools. In addition, selection against senescence should depend on the contribution to population growth arising from physiological investment in offspring at given ages, but offspring are rarely tracked over their entire lives. Here, we use a multigenerational dataset of preindustrial (1732–1860) Finns to describe the association of maternal age at offspring birth with offspring survival and lifetime reproduction. We then conduct longitudinal analyses to understand the drivers of this association. At the population level, offspring lifetime reproductive success (LRS) declined by 22% and individual λ, which falls with delays to reproduction, declined by 45% as maternal age at offspring birth increased from 16 to 50 years. These results were mediated by within‐mother declines in offspring survival and lifetime reproduction. We also found evidence for modifying effects of offspring sex and maternal socioeconomic status. We suggest that our results emerge from the interaction of physiological with social drivers of offspring LRS, which further weakens selection on late‐age reproduction and potentially molds the rate of senescence in humans.     

Laboratory relationships between adult lifetime reproductive success and fitness surrogates in a Drosophila littoralis population

The difficulties in measuring total fitness of individuals necessitate the use of fitness surrogates in ecological and evolutionary studies. These surrogates can be different components of fitness (e.g. survival or fecundity), or proxies more uncertainly related to fitness (e.g. body size or growth rate). Ideally, fitness would be measured over the lifetime of individuals; however, more convenient short-time measures are often used. Adult lifetime reproductive success (adult LRS) is closely related to the total fitness of individuals, but it is difficult to measure and rarely included in fitness estimation in experimental studies. We explored phenotypic correlations between female adult LRS and various commonly used fitness components and proxies in a recently founded laboratory population of Drosophila littoralis. Noting that survival is usually higher in laboratory conditions than in nature, we also calculated adjusted adult LRS measures that give more weight to early reproduction. The lifetime measures of fecundity, longevity, and offspring viability were all relatively highly correlated with adult LRS. However, correlations with short-time measures of fecundity and offspring production varied greatly depending on the time of measurement, and the optimal time for measurement was different for unadjusted compared to adjusted adult LRS measures. Correlations between size measures and adult LRS varied from weak to modest, leg size and female weight having the highest correlations. Our results stress the importance of well-founded choice of fitness surrogates in empirical research.     

Natural selection on age-specific fertilities in human females: comparison of individual-level fitness measures.

Lifetime reproductive success and timing of reproduction are key components of life-history evolution. To understand the evolution of reproductive schedules, it is important to use a measure of fitness that is sensitive both to reproductive quantity and reproductive timing. There is a contradiction between the theory, which mainly focuses on the rate measures of fitness (r and lambda), and empirical studies, which mainly use lifetime reproductive success (LRS), or some of its correlates, as a fitness measure. We measured phenotypic selection on age-specific fertilities in three pre-modern human populations using individually estimated finite rate of increase, er (lambda). We found that lambda and lifetime reproductive success ranked individuals differently according to their fitness: for example, a female giving birth to four children at a young age may actually have a higher fitness than a female giving birth to six children at a greater age. Increase in fertility at the young age classes (15-19 years) was favoured by selection, but the intensity of selection on fertility was higher in the older age classes (20-30 years), where the variance in fertility was highest. Hence, variation in fertility in the older age classes (20-30) was actually responsible for most of the observed variation in fitness among the individuals. Additionally, more than 90% of variation in fitness (lambda) was attributable to individual differences in LRS, whereas only about 5% of all variation in fitness was due to differences in the reproductive schedule. The rate-sensitive fitness measure did not significantly challenge the importance of total fertility as a component of fitness in humans. However, the rate-sensitive measure clearly allowed more accurate estimation of individual fitness, which may be important for answering some more specific questions.     

Lifetime reproductive success of female mountain gorillas

Studies of lifetime reproductive success (LRS) are important for understanding population dynamics and life history strategies, yet relatively little information is available for long-lived species. This study provides a preliminary assessment of LRS among female mountain gorillas in the Virunga volcanoes region. Adult females produced an average of 3.6 ± 2.1 surviving offspring during their lifetime, which indicates a growing population that contrasts with most other great apes. The standardized variance in LRS (variance/mean(2) = 0.34) was lower than many other mammals and birds. When we excluded the most apparent source of environmental variability (poaching), the average LRS increased to 4.3 ± 1.8 and the standardized variance dropped in half. Adult lifespan was a greater source of variance in LRS than fertility or offspring survival. Females with higher LRS had significantly longer adult lifespans and higher dominance ranks. Results for LRS were similar to another standard fitness measurement, the individually estimated finite rate of increase (λ(ind) ), but λ(ind) showed diminishing benefits for greater longevity.     

Skewed distributions of lifetime reproductive success: beyond mean and variance

Lifetime reproductive performance is quantified here by the LRS (lifetime reproductive success), the random number of offspring an individual produces over its lifetime. Many field studies find that distributions of LRS among individuals are non‐normal, zero‐inflated and highly skewed. These results beg the question, what is the distribution of LRS predicted by demographic models when the only source of randomness is demographic stochasticity? Here we present the first exact analysis of the probability distribution of LRS for species described by age + stage models; our analysis starts with estimated vital rates. We illustrate with three examples: the Hadza, human hunter‐foragers (age‐only), the evergreen tree Tsuga canadensis (stage‐only) and Roe deer, Capreolus capreolus (age + stage). For each we obtain the exact distribution of LRS, but also calculate and discuss the first three moments. Our results point to important questions about how such LRS distributions affect natural selection, and life history evolution.     

Sex‐specific pathways of parental age effects on offspring lifetime reproductive success in a long‐lived seabird

The conditions under which individuals are reared vary and sensitivity of offspring to such variation is often sex‐dependent. Parental age is one important natal condition with consequences for aspects of offspring fitness, but reports are mostly limited to short‐term fitness consequences and do not take into account offspring sex. Here we used individual‐based data from a large colony of a long‐lived seabird, the common tern Sterna hirundo, to investigate longitudinal long‐term fitness consequences of parental age in relation to both offspring and parental sex. We found that recruited daughters from older mothers suffered from reduced annual reproductive success. Recruited sons from older fathers were found to suffer from reduced life span. Both effects translated to reductions in offspring lifetime reproductive success. Besides revealing novel sex‐specific pathways of transgenerational parental age effects on offspring fitness, which inspire studies of potential underlying mechanisms, our analyses show that reproductive senescence is only observed in the common tern when including transgenerational age effects. In general, our study shows that estimates of selective pressures underlying the evolution of senescence, as well as processes such as age‐dependent mate choice and sex allocation, will depend on whether causal transgenerational effects exist and are taken into account.     

Male‐induced costs of mating for females compensated by offspring viability benefits in an insect

Sexual conflict facilitates the evolution of traits that increase the reproductive success of males at the expense of components of female fitness. Theory suggests that indirect benefits are unlikely to offset the direct costs to females from antagonistic male adaptations, but empirical studies examining the net fitness pay‐offs of the interaction between the sexes are scarce. Here, we investigate whether matings with males that invest intrinsically more into accessory gland tissue undermine female lifetime reproductive success (LRS) in the cricket Teleogryllus oceanicus. We found that females incur a longevity cost of mating that is proportional to the partner’s absolute investment into the production of accessory gland products. However, male accessory gland weight positively influences embryo survival, and harmful ejaculate‐induced effects are cancelled out when these are put in the context of female LRS. The direct costs of mating with males that sire offspring with higher viability are thus compensated by direct and possibly indirect genetic benefits in this species.     

Facultative Sex Allocation and Sex‐Specific Offspring Survival in Barrow's Goldeneyes

Sex allocation theory predicts that females should bias their reproductive investment towards the sex generating the greatest fitness returns. The fitness of male offspring is often more dependent upon maternal investment, and therefore, high‐quality mothers should invest in sons. However, the local resource competition hypothesis postulates that when offspring quality is determined by maternal quality or when nest site and maternal quality are related, high‐quality females should invest in the philopatric sex. Waterfowl – showing male‐biased size dimorphism but female‐biased philopatry – are ideal for differentiating between these alternatives. We utilized molecular sexing methods and high‐resolution maternity tests to study the occurrence and fitness consequences of facultative sex allocation in Barrow's goldeneyes (Bucephala islandica). We determined how female structural size, body condition, nest‐site safety and timing of reproduction affected sex allocation and offspring survival. We found that the overall sex ratio was unbiased, but in line with the local resource competition hypothesis, larger females produced female‐biased broods and their broods survived better than those of smaller females. This bias occurred despite male offspring being larger and tending to have lower post‐hatching survival. The species shows strong female breeding territoriality, so the benefit of inheriting maternal quality by philopatric daughters may exceed the potential mating benefit for sons of high‐quality females.     

Single-generation estimates of individual fitness as proxies for long-term genetic contribution

Individual fitness is a central evolutionary concept, but the question of how it should be defined in empirical studies of natural selection remains contentious. Using founding cohorts from long-term population studies of two species of individually marked birds (collared flycatcher Ficedula albicollis and Ural owl Strix uralensis), we compared a rate-sensitive (lambdaind) and a rate-insensitive (lifetime reproductive success [LRS]) estimate of individual fitness with an estimate of long-term genetic fitness. The latter was calculated as the number of gene copies present in the population after more than two generations, as estimated by tracing genetic lineages and accounting for the fact that populations were not completely closed. When counting fledglings, rate-insensitive estimates of individual fitness correlated better than rate-sensitive estimates with estimated long-term genetic contribution. When counting recruits, both classes of estimates performed equally well. The results support the contention that simple, rate-insensitive measures of fitness, such as LRS, provide a valid and good estimate of fitness in evolutionary studies of natural populations.     

Population Dynamics of Evolutionary Change: Demographic Parameters as Indicators of Fitness

I evaluated demographic parameters as indicators of fitness by calculating the net reproductive rate (R₀), exponential rate of change (r), lifetime reproductive success (LRS), and Malthusian parameter (m) for nine genotypes and four phenotypes (two alleles at each of two independent loci) of an age-structured population. The given starting conditions included age-specific survival rates of males and females and age-specific fecundity of females for each genotype (to simplify the problem I presumed no differences in survivorship or fecundity of genotypes with the same phenotype) and the same age structure for each genotype. The prevailing genotype had the greatestm, but it did not have the greatestr,R₀, or LRS, or even the greatest survivorship of either juveniles or adults, or the greatest fecundity. This result indicates thatmis the only correct measure of fitness (i.e., as a predictor of which genotype should prevail from among a group of genotypes) and that comparisons ofr,R₀, LRS, juvenile or adult survival rates, or fecundity may be misleading indicators of which genotype should prevail (i.e., be most “fit”) over time (i.e., be selected for).     

Mhc‐linked survival and lifetime reproductive success in a wild population of great tits

Major histocompatibility complex (Mhc) genes are frequently used as a model for adaptive genetic diversity. Although associations between Mhc and disease resistance are frequently documented, little is known about the fitness consequences of Mhc variation in wild populations. Further, most work to date has involved testing associations between Mhc genotypes and fitness components. However, the functional diversity of the Mhc, and hence the mechanism by which selection on Mhc acts, depends on how genotypes map to the functional properties of Mhc molecules. Here, we test three hypotheses that relate Mhc diversity to fitness: (i) the maximal diversity hypothesis, (ii) the optimal diversity hypothesis and (iii) effect of specific Mhc types. We combine mark–recapture methods with analysis of long‐term breeding data to investigate the effects of Mhc class I functional diversity (Mhc supertypes) on individual fitness in a wild great tit (Parus major) population. We found that the presence of three different Mhc supertypes was associated with three different components of individual fitness: survival, annual recruitment and lifetime reproductive success (LRS). Great tits possessing Mhc supertype 3 experienced higher survival rates than those that did not, whereas individuals with Mhc supertype 6 experienced higher LRS and were more likely to recruit offspring each year. Conversely, great tits that possessed Mhc supertype 5 had reduced LRS. We found no evidence for a selective advantage of Mhc diversity, in terms of either maximal or optimal supertype diversity. Our results support the suggestion that specific Mhc types are an important determinant of individual fitness.     

Heritability of individual fitness in female macaques

Heritability of fitness is an important parameter for evolutionary studies, but it is controversial and difficult to estimate this quantitative genetic statistic. I compare two single-generation proxies of individual fitness estimated from demographic information (lifetime reproductive success, LRS; and individual finite rate of increase, individual λ) and lifespan for the female members of a free-ranging population of rhesus macaques (Macaca mulatta). All three variables have moderate heritabilities (λ = 0.36, LRS = 0.38, lifespan = 0.43) that are consistently depressed when non-reproductive individuals are censored from the analysis. This reduction suggests a large portion of the genetic variation in the fitness proxies is due to survival to reproductive age and commencement of reproduction in this population. This may be related to relatively benign, homogeneous environmental conditions. Any time gaps in modeling an animal’s life cycle can introduce similar inaccuracies in heritability of fitness proxies, although the direction of error is likely to vary with environmental conditions. Genetic correlations between the three variables were all indistinguishable from +1 implying no independent genetic variation. The similarity of heritability estimates for λ and LRS and strong genetic correlations are attributed to the dominance of adult lifespan in determining fitness for female macaques which are slow-reproducing by mammalian standards. While the heritabilities of both proxies were similar in this study, they should both be estimated when possible because they may provide different information, particularly in taxa with larger broods.     

POSTZYGOTIC ISOLATION OVER MULTIPLE GENERATIONS OF HYBRID DESCENDENTS IN A NATURAL HYBRID ZONE: HOW WELL DO SINGLE‐GENERATION ESTIMATES REFLECT REPRODUCTIVE ISOLATION?

Understanding speciation depends on an accurate assessment of the reproductive barriers separating newly diverged populations. In several taxonomic groups, prezygotic barriers, especially preferences for conspecific mates, are thought to play the dominant role in speciation. However, the importance of postzygotic barriers (i.e., low fitness of hybrid offspring) may be widely underestimated. In this study, we examined how well the widely used proxy of postzygotic isolation (reproductive output of F₁ hybrids) reflects the long‐term fitness consequences of hybridization between two closely related species of birds. Using 40 species‐specific single nucleotide polymorphism (SNP) markers, we genotyped a mixed population of collared and pied flycatchers (Ficedula albicollis and F. hypoleuca) to identify grand‐ and great grand‐offspring from interspecific crosses to derive an accurate, multigeneration estimate of postzygotic isolation. Two independent estimates of fitness show that hybridization results in 2.4% and 2.7% of the number of descendents typical of conspecific pairing. This postzygotic isolation was considerably stronger than estimates based on F₁ hybrids. Our results demonstrate that, in nature, combined selection against hybrids and backcrossed individuals may result in almost complete postzygotic isolation between two comparatively young species. If these findings are general, postzygotic barriers separating hybridizing populations may be much stronger than previously thought.     

Producing sons reduces lifetime reproductive success of subsequent offspring in pre-industrial Finns

Life-history theory states that reproductive events confer costs upon mothers. Many studies have shown that reproduction causes a decline in maternal condition, survival or success in subsequent reproductive events. However, little attention has been given to the prospect of reproductive costs being passed onto subsequent offspring, despite the fact that parental fitness is a function of the reproductive success of progeny. Here we use pedigree data from a pre-industrial human population to compare offspring life-history traits and lifetime reproductive success (LRS) according to the cost incurred by each individual's mother in the previous reproductive event. Because producing a son versus a daughter has been associated with greater maternal reproductive cost, we hypothesize that individuals born to mothers who previously produced sons will display compromised survival and/or LRS, when compared with those produced following daughters. Controlling for confounding factors such as socio-economic status and ecological conditions, we show that those offspring born after elder brothers have similar survival but lower LRS compared with those born after elder sisters. Our results demonstrate a maternal cost of reproduction manifested in reduced LRS of subsequent offspring. To our knowledge, this is the first time such a long-term intergenerational cost has been shown in a mammal species.     

batemanater: a computer program to estimate and bootstrap mating system variables based on Bateman's principles

Bateman's principles continue to play a major role in the characterization of genetic mating systems in natural populations. The modern manifestations of Bateman's ideas include the opportunity for sexual selection (i.e. I_s – the variance in relative mating success), the opportunity for selection (i.e. I – the variance in relative reproductive success) and the Bateman gradient (i.e. β_ss – the slope of the least‐squares regression of reproductive success on mating success). These variables serve as the foundation for one convenient approach for the quantification of mating systems. However, their estimation presents at least two challenges, which I address here with a new Windows‐based computer software package called batemanater . The first challenge is that confidence intervals for these variables are not easy to calculate. batemanater solves this problem using a bootstrapping approach. The second, more serious, problem is that direct estimates of mating system variables from open populations will typically be biased if some potential progeny or adults are missing from the analysed sample. batemanater addresses this problem using a maximum‐likelihood approach to estimate mating system variables from incompletely sampled breeding populations. The current version of batemanater addresses the problem for systems in which progeny can be collected in groups of half‐ or full‐siblings, as would occur when eggs are laid in discrete masses or offspring occur in pregnant females. batemanater has a user‐friendly graphical interface and thus represents a new, convenient tool for the characterization and comparison of genetic mating systems.     

Revising traditional theory on the link between plant body size and fitness under competition: evidence from old‐field vegetation

The selection consequences of competition in plants have been traditionally interpreted based on a “size‐advantage” hypothesis – that is, under intense crowding/competition from neighbors, natural selection generally favors capacity for a relatively large plant body size. However, this conflicts with abundant data, showing that resident species body size distributions are usually strongly right‐skewed at virtually all scales within vegetation. Using surveys within sample plots and a neighbor‐removal experiment, we tested: (1) whether resident species that have a larger maximum potential body size (MAX) generally have more successful local individual recruitment, and thus greater local abundance/density (as predicted by the traditional size‐advantage hypothesis); and (2) whether there is a general between‐species trade‐off relationship between MAX and capacity to produce offspring when body size is severely suppressed by crowding/competition – that is, whether resident species with a larger MAX generally also need to reach a larger minimum reproductive threshold size (MIN) before they can reproduce at all. The results showed that MIN had a positive relationship with MAX across resident species, and local density – as well as local density of just reproductive individuals – was generally greater for species with smaller MIN (and hence smaller MAX). In addition, the cleared neighborhoods of larger target species (which had relatively large MIN) generally had – in the following growing season – a lower ratio of conspecific recruitment within these neighborhoods relative to recruitment of other (i.e., smaller) species (which had generally smaller MIN). These data are consistent with an alternative hypothesis based on a ‘reproductive‐economy‐advantage’ – that is, superior fitness under competition in plants generally requires not larger potential body size, but rather superior capacity to recruit offspring that are in turn capable of producing grand‐offspring – and hence transmitting genes to future generations – despite intense and persistent (cross‐generational) crowding/competition from near neighbors. Selection for the latter is expected to favor relatively small minimum reproductive threshold size and hence – as a tradeoff – relatively small (not large) potential body size.