Inbreeding,fluctuating asymmetry,and ejaculate quality in an endangered ungulate.

An ever-increasing number of species are suffering marked reductions in population size as a consequence of human activities. To understand the impact of these changes it is essential to assess how small population size affects individual fitness and the viability of populations. This issue acquires special relevance among endangered species in which numbers have decreased to such an extent that captive breeding must be established with a few founders. A major risk associated with small population size is inbreeding depression. The effects of inbreeding upon male reproductive traits are the subject of an ongoing controversy, since the evidence linking lack of genetic variability and poor ejaculate quality at the population level has been criticized recently by several authors. We report that among Gazella cuvieri males, inbreeding coefficient shows a strong inverse relationship with ejaculate quality. Furthermore, the degree of fluctuating asymmetry is positively related to the coefficient of inbreeding and negatively related to the proportion of normal sperm, suggesting that it is a reliable indicator of genetic stress and of ejaculate quality.     

Kinship,sex, and fitness in a Caribbean community

Patterns of human kinship commonly involve preferential treatment of relatives based on lineal descent (lineages) rather than degree of genetic relatedness (kindreds), presenting a challenge for inclusive fitness theory. Here, we examine effects of lineage and kindred characteristics on reproductive success (RS) and number of grandchildren for 130 men and 124 women in a horticultural community on Dominica. Kindreds had little effect on fitness independently of lineage characteristics. Fitness increased with the number of lineal relatives residing in the community but decreased beyond an apparently optimal lineage size, suggesting resource enhancement and competition among kin. Female-biased patrilineage sex ratio was positively associated with men’s fitness, while male-biased matrilineage sex ratio was positively associated with women’s fitness. Number of brothers in the community was negatively associated with men’s, but not women’s, fitness. Parents and number of sisters had no effect on either male or female reproduction; however, women with younger sisters had higher RS, suggesting benefits of kin support for childcare. In sum, imposed norms for lineage social organization may enhance lineal ancestors’ inclusive fitness at a cost to individual inclusive fitness. Research was supported by grants from the National Science Foundation (BNS 8920569 and SBR 9205373); the University of Missouri Research Board to MVF; the Earthwatch Center for Field Research to MVF, Marsha B. Quinlan, and RJQ; and the B.S.U. Center for International Programs and Office of Academic Research and Sponsored Programs to RJQ. Marsha Quinlan and Napoleon Chagnon provided valuable advice on earlier drafts. Ed Hagen gave generous help with Descent software for kinship analysis. Many friends, teachers, and consultants in Bwa Mawego contributed generously to this study: the Durand clan—Juranie, Jonah, Elford, Induria, Margelia, Eugenia, Lillia, Elquimedo, Zexia, Delfine, Wilford, Nathalie, and Sarah; the Warringtons—Martina, Amatus, Onia, Belltina, Zabius, Sarah-Gene, and Heckery; the Laudats—Eddie, Benedict, and Dellie; the Laurents—Aron and Tito; the Lewises—Eddie, Melanie, Eulina, Spliffy, Ganjala, Julina, Jalina, and Marietta; Franklin Vigilante; Lawrence Prosper; Edmund Sanderson; Alex and Tita Alie; and especially Mistress Didi and Mr. McField Coipel. Rob Quinlan is Assistant Professor of Anthropology at Ball State University. His main interests include human evolutionary ecology, reproductive development, parental care, kinship, and medical anthropology. He has conducted fieldwork in Dominica since 1993. Mark Flinn is Associate Professor of Anthropology and Psychological Sciences at the University of Missouri-Columbia. His main interests include evolutionary theory, childhood stress, family relationships, and health. He has conducted fieldwork in Dominica every year since 1987.     

Men in the demographic transition

Women’s fertility is the focus of most demographic analyses, for in most mammals, and in many preindustrial societies, variance in male fertility, while an interesting biological phenomenon, is irrelevant. Yet in monogamous societies, the reproductive ecology of men, as well as that of women, is important is creating reproductive patterns. In nineteenth-century Sweden, the focus of this study, male reproductive ecology responded to resource conditions: richer men had more children than poorer men. Men’s fertility also interacted with local and historical factors in complex ways to have significant impact on population growth. As a result, “the” demographic transition was local, and locally reversible, in Sweden. Results cannot be simply translated from nineteenth-century studies to current attempts to promote fertility decline, because today, male and female resource-fertility curves differ in shape, not only in magnitude. When we translate studies of fertility decline, it is important to study individual fertility and to discern whether, in any particular case, male and female patterns are similar. Bobbi S. Low is Professor of Resource Ecology at the School of Natural Resources and Environment. Her background is in behavioral and evolutionary ecology and her current research interests are human sex differences in risk-taking and resource use.     

PATERNITY ANALYSIS IN A NATURAL POPULATION OF ASCLEPIAS EXALTATA: MULTIPLE PATERNITY,FUNCTIONAL GENDER,AND THE “POLLEN-DONATION HYPOTHESIS”

Recently, some evolutionary biologists have argued that selection on the male component of fitness shapes the evolution of reproductive characters in angiosperms. Floral features, such as inflorescence size, that lead to increased insect visitation without a concomitant increase in seed production are viewed as adaptations to enhance the probability of fathering seeds on other plants. In tests of this “pollen donation hypothesis,” male reproductive success has usually been measured indirectly by flower production, pollinator visitation, or pollen removal. We tested the pollen donation hypothesis directly by quantifying the number of seeds sired by individual genotypes in a natural population of poke milkweed, Asclepias exaltata, in southwestern Virginia. Multiple paternity was low within fruits, a fact which allowed us to use genotypes of progeny arrays to identify a unique pollen parent for 85% of the fruits produced in the population. Seeds sired (male success) and seeds produced (female success) were significantly correlated with flower number per plant (for male success, r = 0.32, P > 0.05; for female success, r = 0.66, P > 0.001). While the number of pollinaria removed, the usual estimator of male success in milkweeds, was highly correlated with numbers of seeds sired (r = 0.47; P > 0.001), it was even more highly correlated with numbers of seeds produced (r = 0.71, P > 0.001). Analysis of functional gender indicated that plants with many flowers did not behave primarily as males. In fact, individuals with the highest total reproductive success contributed equally as males and females. Furthermore, estimates of gender based on numbers of flowers produced or pollinaria removed overestimated the number of functional males in the population. In pollen-limited species, such as many milkweeds, proportional increases in both male and female reproductive success indicate the potential for selection to shape the evolution of large floral displays through both male and female functions.     

Fitness and extra-group reproduction in male Verreaux's sifaka: An analysis of reproductive success from 1989-1999

Adult males in social groups often compete with other male group members for access to adult females. In some primate species, males also seek mating opportunities in neighboring social groups. Such extra-group fertilizations (EGFs) provide an additional source of variation in male fitness. This additional component of fitness provided by EGFs must be incorporated into analyses that investigate sources of variation in male lifetime reproductive success. In this study, a model is analyzed in which male fitness over a 10-year sample period is decomposed into additive and multiplicative variance and covariance components. The data come from an ongoing study of a wild population of Verreaux's sifaka (Propithecus verreauxi verreauxi) located at Beza Mahafaly Special Reserve, Southwest Madagascar. Paternity and demographic data for 134 males are used to decompose male fitness into the following three multiplicative components: reproductive lifespan during sample period, fertility, and offspring survival. These multiplicative components are estimated for males reproducing within their resident groups plus (i.e., the additive portion) for males reproducing in neighboring social groups. The analysis shows that variation in fertility makes the largest contribution to variation in total fitness, followed by variation in amount of time spent in sample period (which is a proxy of total reproductive lifespan) and variation in offspring survival. EGFs contribute an important source of variation to male fitness, and numerous factors enhance the opportunities for EGFs in male sifaka. These include female choice, a high degree of home range overlap, and a limited mating season.     

Low birth weight, maternal birth-spacing decisions, and future reproduction

The aim of this study is an analysis of the possible adaptive consequences of delivery of low birth weight infants. We attempt to reveal the cost and benefit components of bearing small children, estimate the chance of the infants’ survival, and calculate the mothers’ reproductive success. According to life-history theory, under certain circumstances mothers can enhance their lifetime fitness by lowering the rate of investment in an infant and/or enhancing the rate of subsequent births. We assume that living in a risky environment and giving birth to a small infant may involve a shift from qualitative to quantitative production of offspring. Given high infant mortality rates, parents will have a reproductive interest in producing a relatively large number of children with a smaller amount of prenatal investment. This hypothesis was tested among 650 Gypsy and 717 non-Gypsy Hungarian mothers. Our study has revealed that 23.8% of the Gypsy mothers had low birth weight (<2,500 g) children, whose mortality rate is very high. These mothers also had more spontaneous abortions and stillbirths than those with normal weight children. As a possible response to these reproductive failures, they shortened birth spacing, gaining 2–4 years across their reproductive lifespan for having additional children. Because of the relatively short interbirth intervals, by the end of their fertility period, Gypsy mothers with one or two low birth weight infants have significantly more children than their ethnic Hungarian counterparts. They appear to compensate for handicaps associated with low birth weights by having a larger number of closely spaced children following the birth of one or more infants with a reduced probability of survival. The possible alternative explanations are discussed, and the long-term reproductive benefits are estimated for both ethnic groups.     

Are men carrying the apolipoprotein ε4- or ε2 allele less fertile than ε3ε3 genotypes?

The ɛ3 allele in the human gene coding for apolipoprotein E (apoE) is the most common worldwide, but ɛ4 is probably the ancestral allele. Since apoE is involved in many important biological processes, selection forces could have favoured ɛ3. We hypothesized that apoE genotypes may affect reproductive efficiency, and we therefore compared the distributions of 40-year-old married men with known genotypes by the numbers of their biological children. The distributions were statistically significantly different (P = 0.0026). On average, men with the ɛ3ɛ3 genotype (n = 212) had 1.93 children, men with the ɛ3ɛ4 or ɛ4ɛ4 genotype (n = 105) had 1.50, and men with the ɛ3ɛ2 or ɛ2ɛ2 genotypes (n = 53) had 1.66 children. Of the men in the three groups, 6%, 26% and 19%, respectively, reported being childless. These findings are unlikely to be due to gross error in the reported prevalence of childlessness, differences in socioeconomic status or other likely sources of bias. They are compatible with higher fertility in men with the ɛ3ɛ3 genotype than in those with the other common apoE genotypes. Received: 21 August 1995 / Revised: 25 February 1996     

Impact of male alternative reproductive tactics on female costs of sexual conflict under variation in operational sex ratio and population density

Sexual conflict over mating rate is both pervasive and evolutionarily costly. For females, the lifetime reproductive fitness costs that arise through interactions with potential mates will be influenced by the frequency of such interactions, and the fitness cost of each interaction. Both of these factors are likely to be influenced by variation in operational sex ratio (OSR) and population density. Variation in OSR‐ and density‐dependent male alternative reproductive tactics (ARTs) may be particularly important if the fitness costs that females experience vary with the reproductive tactics that males express. Using a simple model, we consider several examples of OSR‐ and/or density‐dependent variation in male ARTs and the frequency of male–female interactions, and find that variation in the expression of male ARTs has the potential to augment or diminish the costs of frequent male interactions for females. Accurately documenting variation in the expression of male ARTs and associated female fitness costs will benefit future work in this area.     

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.     

Sex allocation in simultaneous hermaphrodites: Trade-offs between sex-specific costs and lifespan

Fitness in self-incompatible simultaneous hermaphrodites incorporates gains and costs from both male and female reproductive function, and evolutionarily stable allocation of gonadal tissue to male or female function depends on these gains and costs. Paradoxically, despite the often equal expected gains but different costs associated with each sex, contributions to expected reproductive success through male and female function must be identical. Whenever allocation costs are unequal and limiting resources are energetically expensive or risky to acquire, these costs must ultimately be paid through reduced survival, resolving the paradox by equally diminishing expected reproductive success as male and as female. Maximizing fitness as lifetime reproductive success – not just reproductive rate alone, as in previous studies – maximizes the product of expected survival time and reproductive rate. The analysis shows how male-biased allocation can thereby arise and generate novel predictions on the relation between intensity of sperm competition and allocation to male function.     

Male-biased sex ratio increases female egg laying and fitness in the housefly, Musca domestica

A biased operational sex ratio (OSR) can have multiple, confounding effects on reproductive fitness. A biased OSR can increase harassment and mating activity directed towards potential mates but may also increase the ability of potential mates to choose a good partner if lower quality mates are screened out through competitive interactions. Additionally, a biased OSR may affect reproductive fitness through changes in male ejaculate content or in female reproductive response. We quantified how a male-biased OSR (1:1, 2:1, or 5:1 male to female) affected the size of a female??s first egg clutch and her offspring??s survivorship in the housefly, Musca domestica. A male-biased OSR increased female fitness: females laid more eggs in their first clutch, had increased offspring survivorship at a 2:1 versus 1:1 OSR, and had equivalent fitness with a 5:1 male to female OSR. Courtship activity increased when the OSR was male-biased but was not a significant predictor of female fitness. Trials where females chose their mates versus trials where a random male was chosen for them had equivalent first clutch sizes and offspring survivorship. These results suggest that there are cryptic effects from a male-biased OSR on female fitness that are most likely driven by pre-copulatory social environment.     

Experimental evolution reveals differences between phenotypic and evolutionary responses to population density

Group living can select for increased immunity, given the heightened risk of parasite transmission. Yet, it also may select for increased male reproductive investment, given the elevated risk of female multiple mating. Trade‐offs between immunity and reproduction are well documented. Phenotypically, population density mediates both reproductive investment and immune function in the Indian meal moth, Plodia interpunctella. However, the evolutionary response of populations to these traits is unknown. We created two replicated populations of P. interpunctella, reared and mated for 14 generations under high or low population densities. These population densities cause plastic responses in immunity and reproduction: at higher numbers, both sexes invest more in one index of immunity [phenoloxidase (PO) activity] and males invest more in sperm. Interestingly, our data revealed divergence in PO and reproduction in a different direction to previously reported phenotypic responses. Males evolving at low population densities transferred more sperm, and both males and females displayed higher PO than individuals at high population densities. These positively correlated responses to selection suggest no apparent evolutionary trade‐off between immunity and reproduction. We speculate that the reduced PO activity and sperm investment when evolving under high population density may be due to the reduced population fitness predicted under increased sexual conflict and/or to trade‐offs between pre‐ and post‐copulatory traits.     

Probiotic Microbes Sustain Youthful Serum Testosterone Levels and Testicular Size in Aging Mice

The decline of circulating testosterone levels in aging men is associated with adverse health effects. During studies of probiotic bacteria and obesity, we discovered that male mice routinely consuming purified lactic acid bacteria originally isolated from human milk had larger testicles and increased serum testosterone levels compared to their age-matched controls. Further investigation using microscopy-assisted histomorphometry of testicular tissue showed that mice consuming Lactobacillus reuteri in their drinking water had significantly increased seminiferous tubule cross-sectional profiles and increased spermatogenesis and Leydig cell numbers per testis when compared with matched diet counterparts This showed that criteria of gonadal aging were reduced after routinely consuming a purified microbe such as L. reuteri. We tested whether these features typical of sustained reproductive fitness may be due to anti-inflammatory properties of L. reuteri, and found that testicular mass and other indicators typical of old age were similarly restored to youthful levels using systemic administration of antibodies blocking pro-inflammatory cytokine interleukin-17A. This indicated that uncontrolled host inflammatory responses contributed to the testicular atrophy phenotype in aged mice. Reduced circulating testosterone levels have been implicated in many adverse effects; dietary L. reuteri or other probiotic supplementation may provide a viable natural approach to prevention of male hypogonadism, absent the controversy and side-effects of traditional therapies, and yield practical options for management of disorders typically associated with normal aging. These novel findings suggest a potential high impact for microbe therapy in public health by imparting hormonal and gonad features of reproductive fitness typical of much younger healthy individuals.     

Sex differences in relationships between habitat use and reproductive performance in Soay sheep (Ovis aries)

The role of habitat use in generating individual variation in fitness has rarely been examined empirically in natural populations of long‐lived mammals, particularly for both sexes simultaneously. This is the case despite the increase in studies attempting to understand evolutionary change in such populations. Using data from the St. Kilda Soay sheep population, we quantified the association between lifetime reproductive performance (lifetime breeding and reproductive success) and the proportion of the home range covered by a key grass species, H. lanatus, for 490 females and 304 males. Increased H. lanatus cover was associated only with increased female lifetime reproductive success, but increased lifetime breeding success for both sexes, arising through increased male longevity and increased female fecundity. This work suggests that improved understanding of the causes and consequences of fitness differences will likely require us to better account for habitat‐derived individual variation, and to do so for the sexes appropriately.     

Associations of esterase 6 allozyme and activity variation with reproductive fitness inDrosophila melanogaster

Previous studies have shown that the esterase 6 (EST6) enzyme ofD. melanogaster is mainly produced in the sperm ejaculatory duct of the adult male and comparisons of wild-type males with laboratory null mutants have suggested that the enzyme plays a role in reproductive fitness. In this study we have compared 18 field-derived lines each isoallelic forEst6 for differences in five components of male reproductive fitness. No consistent fitness differences were found among lines differing in respect of the two major allozyme classes EST6-F and EST6-S, despite other evidence that these two classes are not selectively equivalent in the field. However, differences in reproductive fitness were found among lines differing in the minor mobility variants that segregate within EST6-F and EST6-S. A failure to distinguish among these minor forms may explain the discrepancies in previous studies on the effects of the major EST6 allozymes on reproductive fitness. The most significant associations we have found between EST6 and reproductive fitness were due to variation in EST6 activity levels. Male EST6 activity levels were found to be positively correlated with their time to first mating, negatively correlated with the numbers of eggs laid and progeny produced by their mates, and negatively correlated with the frequency with which their mates remate. We conclude that some EST6 variants differ in components of male reproductive fitness operative in laboratory cultures. However, the evidence for fitness differences is stronger for variants affecting the amount, rather than the structure of the enzyme, and the direction of the differences varies between some of the fitness components tested.     

The number of subordinates moderates intrasexual competition among males in cooperatively breeding meerkats

For dominant individuals in cooperatively breeding species, the presence of subordinates is associated with both benefits (i.e. increased reproductive output and other group-living benefits) and costs (i.e. intrasexual competition on reproduction). The biological market theory predicts that dominant individuals are tolerant to same-sex group members when there are only a few subordinates, so as to maximize their own reproductive success. We investigated factors affecting aggression by dominant males and submission by subordinate males for a cooperatively breeding mammal, meerkats, Suricata suricatta. In this species, reproductive conflict occurs between the dominant male and the non-offspring males. As predicted, the number of subordinates in a group was positively associated with the aggression frequency by the dominant male and with the submission frequency by the subordinate males. Relative to the aggression frequency against male offspring, the frequency of aggression against non-offspring males was comparable in small groups, but was higher in large groups. These results indicate that reproductive conflict is present between the dominant male and the non-offspring males but is moderated in groups with small numbers of subordinates. This study provides an empirical data agreeing with the biological market theory in the context of intrasexual competition in cooperatively breeding species.     

Impact of spatial variation of a crucial prey,the molecricket,on hoopoe territory occupancy and reproduction

Direct benefits accrued from securing a territory of sufficient quality are important determinants of individual fitness and population persistence. Food supply is one of the main factors of animal territory quality, with spatial and temporal variation in prey availability largely dictating reproductive output and thus population dynamics. In a Swiss hoopoe population, molecrickets Gryllotalpa gryllotalpa, the most profitable prey locally, can constitute most of the food biomass delivered to chicks by parents. We first investigated the impact of molecricket prey on hoopoes' fitness‐related traits by quantifying the spatial variation in the food allocation pattern of both male and female parents to chicks across the whole population range; and second, analysed the impact of this prey on current reproduction and, using a 11 yr dataset, on the temporal occupancy rate of each territory. We found considerable but spatially repeatable variation, over the years, of molecricket biomass in the diet provisioned to chicks. This spatial heterogeneity in chicks' diet composition was mirrored both in the history of territory occupancy (2002–2012) and in current reproductive success (2012). Territories with a greater biomass of molecrickets in chicks' diet produced more fledglings in better body condition. Yet, these effects on current reproduction were exclusively demonstrated for male parents, corroborating that paternal provisioning patterns play a predominant role in hoopoe reproductive success. This study demonstrates how a single, very profitable prey species might affect spatial variation in territory settlement and individual reproductive success in a regionally endangered bird species, with potential consequences for its population dynamics and persistence.     

Invasion fitness,inclusive fitness,and reproductive numbers in heterogeneous populations

How should fitness be measured to determine which phenotype or “strategy” is uninvadable when evolution occurs in a group‐structured population subject to local demographic and environmental heterogeneity? Several fitness measures, such as basic reproductive number, lifetime dispersal success of a local lineage, or inclusive fitness have been proposed to address this question, but the relationships between them and their generality remains unclear. Here, we ascertain uninvadability (all mutant strategies always go extinct) in terms of the asymptotic per capita number of mutant copies produced by a mutant lineage arising as a single copy in a resident population (“invasion fitness”). We show that from invasion fitness uninvadability is equivalently characterized by at least three conceptually distinct fitness measures: (i) lineage fitness, giving the average individual fitness of a randomly sampled mutant lineage member; (ii) inclusive fitness, giving a reproductive value weighted average of the direct fitness costs and relatedness weighted indirect fitness benefits accruing to a randomly sampled mutant lineage member; and (iii) basic reproductive number (and variations thereof) giving lifetime success of a lineage in a single group, and which is an invasion fitness proxy. Our analysis connects approaches that have been deemed different, generalizes the exact version of inclusive fitness to class‐structured populations, and provides a biological interpretation of natural selection on a mutant allele under arbitrary strength of selection.     

EXTRA‐PAIR PATERNITY AND THE VARIANCE IN MALE FITNESS IN SONG SPARROWS (MELOSPIZA MELODIA)

The variance in fitness across population members can influence major evolutionary processes. In socially monogamous but genetically polygynandrous species, extra‐pair paternity (EPP) is widely hypothesized to increase the variance in male fitness compared to that arising given the socially monogamous mating system. This hypothesis has not been definitively tested because comprehensive data describing males’ apparent (social) and realized (genetic) fitness have been lacking. We used 16 years of comprehensive social and genetic paternity data for an entire free‐living song sparrow (Melospiza melodia) population to quantify and compare variances in male apparent and realized fitness, and to quantify the contribution of the variances in within‐pair reproductive success (WPRS) and extra‐pair reproductive success (EPRS) and their covariance to the variance in realized fitness. Overall, EPP increased the variance in male fitness by only 0–27% across different fitness and variance measures. This relatively small effect reflected the presence of socially unpaired males with zero apparent and low realized fitness, small covariance between WPRS and EPRS, and large variance in WPRS that was relatively unaffected by EPP. Therefore, although EPP altered individual males’ contributions to future generations, its impact on population‐level parameters such as the opportunity for selection and effective population size was limited.