Estimating reproductive success of primates and other animals with long and incompletely known reproductive life spans

Lifetime reproductive success is difficult to obtain for adequate numbers of wild, long-lived animals because of incomplete knowledge of reproductive life histories and fates of offspring. A procedure is described that provides a standard estimate of lifetime reproductive success from either complete or incomplete reproductive life spans. For this procedure, reproductive success is defined as the following ratio: the number of offspring living to a criterion age in a given time period divided by the number expected for that age and period. The number expected is based upon the mean inter-birth interval of the population, the length of the time period, the age criterion of reproductive success chosen by the researcher (e.g., the average age of menarche), and the probability that an offspring will live to the criterion age. The effect of error upon the estimation of parameters is analyzed using the yellow baboons of Mikumi National Park as an example. The method can be used for both sexes, any litter (clutch) size, any mating system, any mean length of interbirth interval, any age criterion of reproductive success, and any study length that allows a reasonably sized sample of individuals for each of whom a substantial proportion of their reproductive life span is known. © 1992 Wiley-Liss, Inc.     

Lifetime reproductive success, longevity, and reproductive life history of female yellow baboons (Papio cynocephalus) of Mikumi National Park, Tanzania

The relationship between longevity and lifetime reproductive success (LRS) was studied in free-ranging female baboons of Mikumi National Park, Tanzania. A severe population decline occurred between the 12th and 20th years of the study. The total sample consisted of 72 females born and reaching adulthood before the start of the population decline. There were 27 females who were adult at the start of the study and 45 who became adult within the 12 years prior to the decline. The subjects were studied until all 72 were dead and all of their offspring were either dead or at least six years old; this took 24 years. The relationship of longevity to LRS was statistically significant for the total sample and for both sub-samples, with 70% of the total variance in LRS accounted for by longevity. Longevity was linked to LRS via a chain of statistically significant relationships: The longer the life span, the longer the reproductive life; the longer the reproductive life, the more offspring produced; the more offspring produced, the higher the LRS. Mean LRS, life span, and reproductive longevity all differed between the two sub-samples. Since the sub-samples were time-linked to a population decline affecting longevity, either sub-sample separately would fail to reflect the broader picture. This illustrates the importance of appreciable sample sizes from long-term studies in helping understand the dynamics between life history estimates and ecological conditions in variable environments.     

Validity of an estimator of reproductive success

Lifetime reproductive success is a major component of individual fitness and a central dependent variable for the study of natural selection. For long-lived animals, such as apes or baboons, assessment of lifetime reproductive success requires observations of identified individuals in continuous, long-term studies from which it is difficult and often impossible to obtain an adequate sample of necessary reproductive and survival data. This situation can be alleviated by the availability of a valid measure that uses incomplete reproductive histories to estimate the lifetime reproductive success of individuals. The validity of one such estimator was tested by determining if, after 10.5 years of studying free-ranging female baboons, it predicted lifetime reproductive success obtained from full reproductive histories after 21.5 years. Validity was evaluated for seven criteria of success, ranging from the number of a female's live births to the number of her offspring that reached the age of 72 months. Moderate to good prediction of lifetime reproductive success by the estimator was found for criteria of offspring living to 36 months or more. After 10.5 years, complete reproductive life spans were available for only eight females. Using the estimator, analytic potential, via sample representativeness and size, was improved at 10.5 years by an increase from a sample of eight to between 34 and 62, depending upon the criterion used, and at 21.5 years from 39 to 70. With a valid estimator, the opportunity to study lifetime reproductive success of a long-lived species is substantially improved without having to depend upon rarely available, uninterrupted data collection for 20–60 years. Am. J. Primatol. 44:137–145, 1998. © 1998 Wiley-Liss, Inc.     

Female differential allocation in response to extrapair offspring and social mate attractiveness

Renewed debate over what benefits females might gain from producing extra‐pair offspring emphasizes the possibility that apparent differences in quality between within‐pair and extra‐pair offspring are confounded by greater maternal investment in extra‐pair offspring. Moreover, the attractiveness of a female''s social mate can also influence contributions of both partners to a reproductive attempt. Here, we explore the complexities involved in parental investment decisions in response to extra‐pair offspring and mate attractiveness with a focus on the female point of view. Adult zebra finches paired and reproduced in a colony setting. A male''s early‐life diet quality and his extra‐pair reproductive success were used as metrics of his mating attractiveness. Females paired with males that achieved extra‐pair success laid heavier eggs than other females and spent less time attending their nests than their mates or other females. Extra‐pair nestlings were fed more protein‐rich hen''s egg than within‐pair nestlings. Females producing extra‐pair offspring had more surviving sons than females producing only within‐pair offspring. Collectively, results show that females differentially allocate resources in response to offspring extra‐pair status and their social mate''s attractiveness. Females may also obtain fitness benefits through the production of extra‐pair offspring.     

The sexual selection continuum

The evolution of mate choice for genetic benefits has become the tale of two hypotheses: Fisher's 'run-away' and 'good genes', or viability indicators. These hypotheses are often pitted against each other as alternatives, with evidence that attractive males sire more viable offspring interpreted as support for good genes and with a negative or null relationship between mating success of sons and other components of fitness interpreted as favouring the Fisher process. Here, we build a general model of female choice for indirect benefits that captures the essence of both the 'Fisherian' and 'good-genes' models. All versions of our model point to a single process that favours female preference for males siring offspring of high reproductive value. Enhanced mating success and survival are therefore equally valid genetic benefits of mate choice, but their relative importance varies depending on female choice costs. The relationship between male attractiveness and survival may be positive or negative, depending on life-history trade-offs and mating skew. This relationship can change sign in response to increased costliness of choice or environmental change. Any form of female preference is subject to self-reinforcing evolution, and any relationship (or lack thereof) between male display and offspring survival is inevitably an indicator of offspring reproductive values. Costly female choice can be maintained with or without higher offspring survival.     

Dominance and reproductive success in primates

Theoretical models of the relationship between competition and differential reproduction in primates share the premise that agonistic dominance hierarchies determine differential access to those limited resources which are essential to reproduction. In particular, the priority-of-access-to-estrous-female model is based on the postulate that high rank in males enhances reproductive success. Tests for a correlation between rank and reproductive success in males have produced mixed results. Problems in measuring male reproductive success and in conceptualizing dominance systems are implicated in the diversity of conclusions reached. Other attributes which affect reproductive success have been proposed, and alternative models of mating systems, based on the concepts of reproductive strategies, social skills, and life histories have also been developed. Studies of differential reproduction in female primates are fewer, but have the advantage over male studies of directly measuring infant production and offspring survival. Research on the relationship between rank and reproductive success in females has shown that under conditions of low resource availability, subordinate females sometimes suffer reduced fecundity and infant survival as a result of restricted access to food and water. Under conditions of social stress, low-ranking females may suffer from disruption of their reproductive cycles, resulting in lowered fecundity. Dominant females may also incur reproductive costs as well as benefits for their social position. Better insights into the relationship between dominance and reproduction are potentially offered by improved genetic paternity measures, new models of social and demographic processes, and the recent availability of life history data from field studies.     

Does catch and release affect the mating system and individual reproductive success of wild Atlantic salmon (Salmo salar L.)?

In this study, we documented the breeding system of a wild population of Atlantic salmon (Salmo salar L.) by genetically sampling every returning adult and assessed the determinants of individual fitness. We then quantified the impacts of catch and release (C&R) on mating and reproductive success. Both sexes showed high variance in individual reproductive success, and the estimated standardized variance was higher for males (2.86) than for females (0.73). We found a weak positive relationship between body size and fitness and observed that fitness was positively correlated with the number of mates, especially in males. Mature male parr sired 44% of the analysed offspring. The impact of C&R on the number of offspring was size dependent, as the reproductive success of larger fish was more impaired than smaller ones. Also, there was an interactive negative effect of water temperature and air exposure time on reproductive success of C&R salmon. This study improves our understanding of the complex reproductive biology of the Atlantic salmon and is the first to investigate the impact of C&R on reproductive success. Our study expands the management toolbox of appropriate C&R practices that promote conservation of salmon populations and limit negative impacts on mating and reproductive success.     

Males from populations with higher competitive mating success produce sons with lower fitness

Female mate choice can result in direct benefits to the female or indirect benefits through her offspring. Females can increase their fitness by mating with males whose genes encode increased survivorship and reproductive output. Alternatively, male investment in enhanced mating success may come at the cost of reduced investment in offspring fitness. Here, we measure male mating success in a mating arena that allows for male–male, male–female and female–female interactions in Drosophila melanogaster. We then use isofemale line population measurements to correlate male mating success with sperm competitive ability, the number of offspring produced and the indirect benefits of the number of offspring produced by daughters and sons. We find that males from populations that gain more copulations do not increase female fitness through increased offspring production, nor do these males fare better in sperm competition. Instead, we find that these populations have a reduced reproductive output of sons, indicating a potential reproductive trade‐off between male mating success and offspring quality.     

Life span,reproductive output,and reproductive opportunity in captive Goeldi's monkeys (Callimico goeldii)

In the absence of long‐term field studies, demographic and reproductive records from animals housed in zoos and research laboratories are a valuable tool for the study of life history variables relating to reproduction. In this study, we analyzed studbook records of more than 2,000 individuals born over a 40‐year period (1965–2004) to describe life history patterns of captive Goeldi's monkeys (Callimico goeldii) housed in North America and Europe. Using Kaplan–Meier survival analysis methods, we found the mean life span to be 5.5 years. The rate of infant mortality, defined as death before 30 days, was approximately 30%, with European animals being more likely to survive infancy than North American animals. When individuals surviving at least 1.5 years are considered, lifetime reproductive output averaged 3.5 offspring, yet more than one‐third of individuals did not produce any offspring. Using a smaller dataset of individuals with known pairing histories, we developed a measure of opportunity for reproduction (OFR), which represented the total time an individual was known to be housed with a potential mate. For both sexes, we found that the correlation between OFR and number of offspring produced was much higher than the correlation between life span and number of offspring produced. This result highlights the importance of taking into account an individual's OFR. As a whole, our findings help characterize the life histories of captive Goeldi's monkeys and emphasize the impact management practices may have on reproductive success. Zoo Biol 29:1–15, 2010. © 2009 Wiley‐Liss, Inc.     

SEX-RATIO MANIPULATION IN RESPONSE TO HOST SIZE BY THE PARASITOID WASP SPALANGIA CAMERONI: A LABORATORY STUDY

The prediction of Charnov et al.'s (1981) host-size model that there should be a negative relationship between host size and wasp sex ratio (proportion sons) was supported for Spalangia cameroni, a solitary parasitoid wasp. The relationship was shown to be a result of offspring sex manipulation by females in response to host size rather than a result of differential mortality of the sexes. A major assumption of the host-size model is that host size has a greater effect on the ultimate reproductive success of emerging female wasps than of males. This assumption was not supported. Host size had a positive effect on the size of both male and female S. cameroni. However, neither host size nor wasp size affected longevity, production of offspring by females, or ability of males to compete for mates. Host size may differentially affect the reproductive success of female and male wasps through effects on other aspects of reproductive success. Tests of the assumptions of offspring sex-ratio manipulation hypotheses are scarce but critical, not only for parasitoid wasps, but also for other organisms.     

Choosing mates: good genes versus genes that are a good fit

Female choice for male ornamental traits is widely accepted as a mechanism by which females maximize their reproductive success and/or offspring quality. However, there is an increasing empirical literature that shows a fitness benefit of genetic diversity and a tendency for females to use genetic dissimilarity as a criterion for mate choice. This genetic compatibility hypothesis for female mate choice presents a paradox. How can females use both an absolute criterion, such as male ornamentation, and a relative criterion, such as genetic dissimilarity, to choose their mates? Here, we present potential solutions for this dilemma and the empirical evidence supporting them. The interplay between these two contrasting forms of female mate choice presents an exciting empirical and theoretical challenge for evolutionary ecologists.     

Alternative reproductive tactics in atlantic salmon: factors affecting mature parr success

In Atlantic salmon, as in most salmonids, males can mature early in the life cycle, as small freshwater fish, termed parr, and/or undergo a sea migration before maturing as full-size adults. The alternative life histories are contingent on environmental and social circumstances, such as growth rate, territory quality or any other factor that affects the individual''s state. In order to model the choice of life history in this group of commercially valuable species, it is necessary to understand not only the relative contribution of the different male types to subsequent generations, but also to know the factors that affect reproductive success in each type. In this paper we present the results of a study designed to investigate the factors that affect the reproductive success of mature parr. We used highly polymorphic minisatellite DNA markers to analyse paternity in a series of mating experiments where the number and body size of parr were manipulated. The fraction of eggs fertilized by mature parr ranged from 26 to 40 per cent, with individual parr fertilizing up to 26 per cent of the eggs. A strong positive correlation was found between parr size and reproductive success. The relative success of parr decreased with increasing parr number. Data from this and other studies on variation in the timing and degree of parr reproductive success are discussed in relation to the evolution of male mating strategies and life history in salmonids.     

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.     

Experience Matters: Females Use Smell to Select Experienced Males for Paternal Care

Mate choice and mating preferences often rely on the information content of signals exchanged between potential partners. In species where a female''s reproduction is the terminal event in life it is to be expected that females choose high quality males and assess males using some honest indicator of male quality. The Nereidid polychaete, Neanthes acuminata, exhibits monogamous pairing and the release of eggs by females terminates her life and larval success relies entirely on a male''s ability to provide paternal care. As such females should have developed reliable, condition-dependent criteria to choose mates to guarantee survival and care for offspring. We show that females actively chose males experienced in fatherhood over others. In the absence of experienced males dominance, as evident from male-male fights, is utilized for mate selection. The preference for experienced males is not affected by previous social interactions between the individuals. We show that the choice of the partner is based on chemical signals demonstrating a ‘scent of experience’ to females providing evidence for the role of chemical signals in sexual selection for paternal care adding to our understanding of the mechanisms regulating condition-dependent mate choice.     

A model for estimating the minimum number of offspring to sample in studies of reproductive success

Molecular parentage permits studies of selection and evolution in fecund species with cryptic mating systems, such as fish, amphibians, and insects. However, there exists no method for estimating the number of offspring that must be assigned parentage to achieve robust estimates of reproductive success when only a fraction of offspring can be sampled. We constructed a 2-stage model that first estimated the mean (μ) and variance (v) in reproductive success from published studies on salmonid fishes and then sampled offspring from reproductive success distributions simulated from the μ and v estimates. Results provided strong support for modeling salmonid reproductive success via the negative binomial distribution and suggested that few offspring samples are needed to reject the null hypothesis of uniform offspring production. However, the sampled reproductive success distributions deviated significantly (χ(2) goodness-of-fit test p value < 0.05) from the known simulated reproductive success distribution at rates often >0.05 and as high as 0.24, even when hundreds of offspring were assigned parentage. In general, reproductive success patterns were less accurate when offspring were sampled from cohorts with larger numbers of parents and greater variance in reproductive success. Our model can be reparameterized with data from other species and will aid researchers in planning reproductive success studies by providing explicit sampling targets required to accurately assess reproductive success.     

Mate choice for major histocompatibility complex genetic divergence as a bet-hedging strategy in the Atlantic salmon (Salmo salar)

Major histocompatibility complex (MHC)-dependent mating preferences have been observed across vertebrate taxa and these preferences are expected to promote offspring disease resistance and ultimately, viability. However, little empirical evidence linking MHC-dependent mate choice and fitness is available, particularly in wild populations. Here, we explore the adaptive potential of previously observed patterns of MHC-dependent mate choice in a wild population of Atlantic salmon (Salmo salar) in Québec, Canada, by examining the relationship between MHC genetic variation and adult reproductive success and offspring survival over 3 years of study. While Atlantic salmon choose their mates in order to increase MHC diversity in offspring, adult reproductive success was in fact maximized between pairs exhibiting an intermediate level of MHC dissimilarity. Moreover, patterns of offspring survival between years 0+ and 1+, and 1+ and 2+ and population genetic structure at the MHC locus relative to microsatellite loci indicate that strong temporal variation in selection is likely to be operating on the MHC. We interpret MHC-dependent mate choice for diversity as a likely bet-hedging strategy that maximizes parental fitness in the face of temporally variable and unpredictable natural selection pressures.     

Mendel’s law reveals fatal flaws in Bateman’s 1948 study of mating and fitness

Bateman’s experimental study of Drosophila melanogaster produced conclusions that are now part of the bedrock premises of modern sexual selection. Today it is the most cited experimental study in sexual selection, and famous as the first experimental demonstration of sex differences in the relationship between number of mates and relative reproductive success. We repeated the experimental methodology of the original to evaluate its reliability. The results indicate that Bateman’s methodology of visible mutations to assign parentage and reproductive success to subject adults is significantly biased. When combined in offspring, the mutations decrease offspring survival, so that counts of mate number and reproductive success are mismeasured. Bateman’s method overestimates the number of subjects with no mates and underestimates the number with one or more mates for both sexes. Here we discuss why Bateman’s paper is important and present additional analyses of data from our monogamy trials. Monogamy trials can inform inferences about the force of sexual selection in populations because in monogamy trials male–male competition and female choice are absent. Monogamy trials also would have provided Bateman with an a priori test of the fit of his data to Mendel’s laws, an unstated, but vital assumption of his methodology for assigning parentage from which he inferred the number of mates per individual subject and their reproductive success. Even under enforced monogamous mating, offspring frequencies of double mutant, single mutant and no mutant offspring were significantly different from Mendelian expectations proving that Bateman’s method was inappropriate for answering the questions he posed. Double mutant offspring (those with a mutation from each parent) suffered significant inviability as did single mutant offspring whenever they inherited their mother’s marker but the wild-type allele at their father’s marker locus. These inviability effects produced two important inaccuracies in Bateman’s results and conclusions. (1) Some matings that actually occurred were invisible and (2) reproductive success of some mothers was under-estimated. Both observations show that Bateman’s conclusions about sex differences in number of mates and reproductive success were unwarranted, based on biased observations. We speculate about why Bateman’s classic study remained without replication for so long, and we discuss why repetition almost 60 years after the original is still timely, necessary and critical to the scientific enterprise. We highlight overlooked alternative hypotheses to urge that modern tests of Bateman’s conclusions go beyond confirmatory studies to test alternative hypotheses to explain the relationship between mate number and reproductive success.     

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.     

An experimental test for body size‐dependent effects of male harassment and an elevated copulation rate on female lifetime fecundity and offspring performance

Many studies investigate the benefits of polyandry, but repeated interactions with males can lower female reproductive success. Interacting with males might even decrease offspring performance if it reduces a female's ability to transfer maternal resources. Male presence can be detrimental for females in two ways: by forcing females to mate at a higher rate and through costs associated with resisting male mating attempts. Teasing apart the relative costs of elevated mating rates from those of greater male harassment is critical to understand the evolution of mating strategies. Furthermore, it is important to test whether a male's phenotype, notably body size, has differential effects on female reproductive success versus the performance of offspring, and whether this is due to male body size affecting the costs of harassment or the actual mating rate. In the eastern mosquitofish Gambusia holbrooki, males vary greatly in body size and continually attempt to inseminate females. We experimentally manipulated male presence (i.e., harassment), male body size and whether males could copulate. Exposure to males had strong detrimental effects on female reproductive output, growth and immune response, independent of male size or whether males could copulate. In contrast, there was a little evidence of a cross‐generational effect of male harassment or mating rate on offspring performance. Our results suggest that females housed with males pay direct costs due to reduced condition and offspring production and that these costs are not a consequence of increased mating rates. Furthermore, exposure to males does not affect offspring reproductive traits.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.