Direct Fitness Benefits Research Articles

COOPERATION IN THE RHIZOSPHERE AND THE “FREE RIDER” PROBLEM

Rhizobial bacteria, endomycorrhizal fungi (also known as arbuscular my- corrhizas), and pseudomonad bacteria associated with plant roots can provide substantial benefits to the plants by fixing nitrogen, supplying phosphorus, or controlling root path- ogens, respectively. A significant fraction of plant photosynthetic carbon may be used by these associated microorganisms, both to support their beneficial activities and for microbial growth and reproduction. Because many microbial individuals are associated with each individual plant, the individual benefit to a microbe that allocates more resources to its own reproduction (thereby allocating less to fixing N 2, supplying P, or producing antifungal metabolites) would exceed its individual loss from any resulting reduction in collective benefits (mainly plant carbon substrates). An initially rare ''free rider'' mutant strain might therefore be expected to displace its more cooperative parental strain. Yet, the mycorrhizal and legume-rhizobium mutualisms have persisted (often coexisting with ''cheating'') for millions of years. This paper discusses the importance of microbial cooperation (with plants and with other microbes) and possible reasons for its evolutionary persistence in the rhi- zosphere. In undisturbed soils, spatial structure can favor kin selection, but this may be counterbalanced by the increased likelihood that future competitors will be among the beneficiaries of current cooperation. In loose associations, direct fitness benefits to micro- organisms may explain the evolutionary persistence of activities (e.g., production of an- tifungal compounds) that can benefit plants as a side effect. In closer, more symbiotic, relationships, host sanctions against individuals or clones that fail to perform their symbiotic function may be more important. New molecular methods and other research tools are facilitating research on this topic, and some of these conclusions soon may be revised.

Genetic niche‐hiking: an alternative explanation for the evolution of flammability

In fire‐prone ecosystems, many plants possess traits that enhance their relative flammability and ecologists have suggested increased flammability could result from natural selection. To date, theoretical models addressing the evolution of flammable characteristics assume that flammable plants realize some direct fitness advantage. In this paper, we explore the idea that enhanced flammability can increase in frequency in a population without any direct fitness benefit to the flammable type. In our model, flammability evolves due to an association between an allele that promotes flammability and alleles at unlinked loci that give high fitness. In analogy to genetic hitchhiking, in which a deleterious allele can invade due to a genetic linkage, we call this process “genetic niche‐hiking,” because the association results from localized niche construction. Specifically, flammable plants sacrifice themselves and their neighbors to produce local fire‐cleared gaps (the constructed niche) in which their offspring are able to continually track an ever‐changing environment. Niche‐hiking requires that mating, dispersal and niche construction all occur locally (i.e. the population is spatially structured), such that offspring are likely to experience the niches their parents construct. Using a spatially‐explicit lattice‐based simulation, we find that increased flammability can evolve despite the “self‐killing” cost of such a trait. Genetic niche‐hiking may also be applicable to the evolution of other traits in spatially structured ecological systems such as plant disease susceptibility and forest tree characteristics that influence gap production.

Direct fitness benefits of group living in a complex cooperative society of carrion crows, Corvus corone corone

The social behaviour of carrion crows varies between populations. In northern Spain cooperatively breeding groups form through delayed natal dispersal and/or immigration of individuals (usually males) into the territory. In this population, carrion crows therefore breed as either unassisted pairs, pairs with nondispersing 1–2-year-old helpers (nondispersers), pairs with immigrant helpers or mixed groups (pairs with both immigrants and nondispersers). We used a microsatellite-based genotyping system to determine the parentage of 57 nestlings (19 broods). Polygamous mating was involved in 26% of the broods and reproduction was shared among group members of both sexes in at least three groups. Immigrants of both sexes can therefore gain access to mates by living in a group, while reproduction is unlikely to involve nondispersers. This implies that nondispersers and immigrants gain different sorts of benefits from group living and helping at the nest. Our genetic data confirmed that nondispersers associated with their parents on the natal territory and therefore that delayed natal dispersal leads to family formation in the carrion crow. Polygamous mating was not found in groups without immigrants, suggesting that, in this population, breeders lose parentage in their brood when sociality is extended beyond the limit of the nuclear family. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Polyandry produces sexy sons at the cost of daughters in red flour beetles.

Female mating with multiple males within a single fertile period is a common phenomenon in the animal kingdom. Female insects are particularly promiscuous. It is not clear why females mate with multiple partners despite several potential costs, such as expenditure of time and energy, reduced lifespan, risk of predation and contracting sexually transmitted diseases. Female red flour beetles (Tribolium castaneum) obtain sufficient sperm from a single insemination to retain fertility for several months. Nonetheless they copulate repeatedly within minutes with different males despite no direct fitness benefits from this behaviour. One hypothesis is that females mate with multiple partners to provide indirect benefits via enhanced offspring fitness. To test this hypothesis, we compared the relative fitness of F(1) offspring from females mated with single males and multiple males (2, 4, 8, or 16 partners), under the condition of relatively high intraspecific competition. We found that a female mating with 16 males enhanced the relative fitness of F(1) males (in two out of three trials) but reduced F(1) females' fitness (in two independent trials) in comparison with singly mated females. We also determined whether several important fitness correlates were affected by polyandry. We found that F(1) males from mothers with 16 partners inseminated more females than F(1) males from mothers with a single partner. The viability of the eggs sired or produced by F(1) males and females from highly polyandrous mothers was also increased under conditions of low intra-specific competition. Thus, the effects of polyandry on F(1) offspring fitness depend on environmental conditions. Our results demonstrated a fitness trade-off between male and female offspring from polyandrous mothers in a competitive environment. The mechanisms and biological significance of this unique phenomenon are discussed.

How important are direct fitness benefits of sexual selection?

Females may choose mates based on the expression of secondary sexual characters that signal direct, material fitness benefits or indirect, genetic fitness benefits. Genetic benefits are acquired in the generation subsequent to that in which mate choice is performed, and the maintenance of genetic variation in viability has been considered a theoretical problem. Consequently, the magnitude of indirect benefits has traditionally been considered to be small. Direct fitness benefits can be maintained without consideration of mechanisms sustaining genetic variability, and they have thus been equated with the default benefits acquired by choosy females. There is, however, still debate as to whether or not males should honestly advertise direct benefits such as their willingness to invest in parental care. We use meta-analysis to estimate the magnitude of direct fitness benefits in terms of fertility, fecundity and two measures of paternal care (feeding rate in birds, hatching rate in male guarding ectotherms) based on an extensive literature survey. The mean coefficients of determination weighted by sample size were 6.3%, 2.3%, 1.3% and 23.6%, respectively. This compares to a mean weighted coefficient of determination of 1.5% for genetic viability benefits in studies of sexual selection. Thus, for several fitness components, direct benefits are only slightly more important than indirect ones arising from female choice. Hatching rate in male guarding ectotherms was by far the most important direct fitness component, explaining almost a quarter of the variance. Our analysis also shows that male sexual advertisements do not always reliably signal direct fitness benefits.

Towards a resolution of the lek paradox.

Genetic benefits in the shape of 'good genes' have been invoked to explain costly female choice in the absence of direct fitness benefits. Little genetic variance in fitness traits is expected, however, because directional selection tends to drive beneficial alleles to fixation. There seems to be little potential, therefore, for female choice to result in genetic benefits, giving rise to the 'lek paradox'. Nevertheless, evidence shows that genetic variance persists despite directional selection and genetic benefits of female choice are frequently reported. A theoretical solution to the lek paradox has been proposed on the basis of two assumptions: that traits are condition-dependent, and that condition shows high genetic variance. The observed genetic variability in sexual traits will be accounted for, because a proportion of the genetic variance in condition will be captured and expressed in the trait. Here we report results from experiments showing that male courtship rate in the dung beetle Onthophagus taurus is a condition-dependent trait that is preferred by females. More importantly, male condition has high genetic variance and is genetically correlated with courtship rate. Our results thereby represent a significant step towards a resolution of the lek paradox.

Fine-scale genetic structuring on Manacus manacus leks.

Leks have traditionally been considered as arenas where males compete to attract females and secure matings. Thus, direct fitness benefits mediated through competition between males to fertilize females have been considered to be the primary force driving the evolution of lekking behaviour. Inclusive fitness benefits mediated through kin selection may also be involved in lek formation and evolution, but to date this theory has been largely ignored. According to kin-selection theory, both reproducing and non-reproducing males may gain indirect inclusive fitness benefits. If females are attracted to larger leks, non-reproducing males add attractiveness to a lek, and therefore, in a genetically structured population, boost the reproductive success of kin. Theory predicts that the attractiveness of leks is plastic, and that males establish themselves on a lek in which the top male, in terms of reproductive success, is a close relative. Here we show that in white-bearded manakins (Manacus manacus), for which larger leks are more attractive to females and so secure the maximum number of matings, there is extraordinary fine-scale genetic structure, with leks being composed of clusters of related kin. We propose that males establish themselves where they find relatives to such an extent that they form groups within leks, and that such behaviour is consistent with kin-selection theory to maximize reproductive success of the group.

Male-biased sex ratio in litters of Alpine marmots supports the helper repayment hypothesis

In a French population of Alpine marmots (Marmota marmota), the sex ratio at weaning was biased in favor of males. This bias also seemed to exist at birth. Under Fisher’s equal allocation principle, this means that daughters should be more costly to produce than sons. Because the Alpine marmot can be considered a cooperative breeding species, we investigated whether the differential cost between sons and daughters may be explained by the helper repayment hypothesis. The Alpine marmot uses social thermoregulation during hibernation, allowing juveniles to better survive over winter. In the study population, juvenile survival during winter increased with group size. More precisely, juvenile survival during winter increased with the number and with the proportion of subordinate males in the hibernating group, but juvenile survival did not depend on the number of subordinate females. As our results did not support alternative hypotheses to explain the observed bias in sex ratio among offspring at emergence, we conclude that the helper repayment hypothesis is the best candidate to explain the observed offspring sex ratio bias in Alpine marmots. By participating in social thermoregulation, subordinate males may repay part of the investment they received from their parents and thus become less costly to produce. We suggest that only subordinate males helped because they may gain direct fitness benefits, whereas subordinate females may only expect indirect fitness benefits from helping. Finally, the offspring sex ratio per individual parent was male biased, but mothers adjusted the size and the sex composition of their litters according to their phenotypic condition as expected from the Trivers-Willard hypothesis. Key words: Alpine marmots, cooperative breeding, helper repayment hypothesis, Marmota marmota, sex ratios. [Behav Ecol 11:507–514 (2000)]

Male parental care, female reproductive success, and extrapair paternity

Birds differ considerably in the degree of male parental care, and it has been suggested that interspecific variation in extrapair paternity is determined by the relative importance of benefits to females from male parental care and good genes from extrapair sires. I estimated the relationship between extrapair paternity and the importance of male parental care for female reproductive success mainly based on male removal studies, using a comparative approach. The reduction in female reproductive success caused by the absence of a male mate was positively correlated with the male contribution to feeding offspring. The frequency of extrapair paternity was negatively related to the reduction in female reproductive success caused by the absence of a mate. This was also the case when potentially confounding variables such as developmental mode of offspring and sexual dichromatism were considered. A high frequency of extrapair paternity occurs particularly in bird species in which males play a minor role in offspring provisioning and in which attractive males provide relatively little parental care. Bird species with frequent extrapair paternity thus appear to be those in which direct fitness benefits from male care are small, females can readily compensate for the absence of male care, and indirect fitness benefits from extrapair sires are important.

Immunocompetence of nestling great tits in relation to rearing environment and parentage

Theoretical models of host–parasite coevolution assume a partially genetic basis to the variability in susceptibility to parasites among hosts, for instance as a result of genetic variation in immune function. However, few empirical data exist for free–living vertebrate hosts to support this presumption. In a cross–fostering experiment with nestling great tits, by comparing nestlings of the same origin we investigated (i) the variance in host resistance against an ectoparasite due to a common genetic origin, (ii) the effect of ectoparasite infestation on cell–mediated immunity and (iii) the variance in cell–mediated immunity due to a common genetic origin. Ectoparasitic hen fleas can impair the growth of nestling great tits and nestling growth was therefore taken as a measure of host susceptibility. A common origin did not account for a significant part of the variation in host susceptibility to fleas. There was no significant overall effect of fleas on nestling growth or cell–mediated immunity, as assessed by a cutaneous hypersensitivity response. A common rearing environment explained a significant part of the variation in cell–mediated immunity among nestlings, mainly through its effect on nestling body mass. The variation in cell–mediated immunity was also related to a common origin. However, the origin–related variation in body mass did not account for the origin–related differences in cell–mediated immunity. The results of the present study thus suggest heritable variation in cell–mediated immunity among nestling great tits.

Reproductive Success and Nest-Site Selection in a Cooperative Breeder: Effect of Experience and a Direct Benefit of Helping

We determined whether nest-site characteristics influence reproductive suc- cess and whether experience influences nest-site selection in a population of cooperatively breeding Long-tailed Tits (Aegithalos caudatus). Nest predation was high; only 17% of breed- ing attempts resulted in fledged young. The height of nests was an important determinant of success; low nests were significantly more successful than high nests. A breeder's age, natal nest site, and breeding experience had no significant effect on nest-site selection. How- ever, failed breeders who helped at the successful nests of conspecifics built subsequent nests lower than nests built prior to their helping experience. Failed breeders who did not help showed no reduction in the height of subsequent nests. Moreover, the subsequent repro- ductive success of failed breeders who helped was significantly higher than that of failed breeders who did not help. We conclude that helpers gain information on nest-site quality through their helping experience and thus gain a direct fitness benefit from their cooperative behavior. We suggest that experience as a helper offers a more reliable cue to nest-site quality than breeding experience because helpers are associated with nests only during the nestling phase when few nests are depredated. In contrast, although successful breeders may expe-

Male parental care, differential parental investment by females and sexual selection

Males play a variable parental role in reproduction, ranging from no male parental care to extensive male care. Females may acquire either direct or indirect fitness benefits from their mate choice, and direct fitness benefits include male parental care. Theoreticians have traditionally emphasized direct fitness benefits to females in species with extensive male parental care. We review the literature and show extensive variation in the patterns of male care, related to the attractiveness of males to females. At one extreme of this continuum, females invest differentially in parental care, investing more when paired with attractive males. The costs of female parental care and other aspects of parental investment may be balanced by benefits in terms of more attractive sons and/or more viable offspring. At the other extreme, in species with extensive direct fitness benefits, males with preferred sexual phenotypes provide the largest relative share of parental care. A comparative study of birds revealed that the extent of the differential female parental investment was directly related to the frequency of extra-pair paternity. Since extra-pair paternity may arise mainly as a consequence of female choice for indirect fitness benefits, this result supports our prediction that differential parental investment is prevalent in species where females benefit indirectly from their mate choice. The consequences for sexual selection theory of these patterns of male care in relation to male attractiveness are emphasized.

Helping-at-the-Nest and Group Size in the Arabian Babbler Turdoides squamiceps

Wright, J. 1998. Helping-at-the-nest and group size in the Arabian Babbler Turdoides squamiceps. - J. Avian Biol. 29: 105-112. The effect of group size on the productivity of communally-breeding bird species has for many years been linked with the various adaptive explanations for helping-at-thenest. This study examines the effect of group size on group provisioning effort and group productivity in the Arabian Babbler Turdoides squamiceps, a species in which helping behaviour is reported to have limited impact on parental reproduction, and has instead been uniquely proposed to operate as a signal within the group to gain social prestige. Contrary to these earlier reports, the present study showed a strong positive and linear effect of group size upon the total number of provisioning visits to the nest and the number of fledglings produced. Larger groups produced larger numbers of young, although individual fledging mass did not decrease with this increase in brood size. Fewer faecal sacs were removed per visit in nests with larger broods, and this was the only variable for which an initial positive effect of group size could be explained by the potentially confounding effect of brood size. In addition, individual provisioning effort was reduced in larger groups, both in terms of number of nest visits and the size of prey items delivered per visit. Although these data were collected over only three breeding seasons, the group sizes and breeding conditions involved are broadly representative of this population during the previous 25 years of records. These results therefore suggest that, under the majority of circumstances, helping-at-the-nest in Arabian Babblers has a positive and linear effect on the reproductive success of parents, as well as substantially reducing the provisioning effort required of other group members. Groups were nearly always made up of closely related individuals, and so these data are consistent with kin selection. Helpers gain indirect fitness benefits from the increased reproductive success of nests, as well as potentially reducing the survival costs of chick feeding for adult relatives. The possibility of direct fitness benefits from helping, especially regarding pseudoreciprocity and adaptive group augmentation, is also discussed with reference to the evolution of helping behaviour and group-living in the Arabian Babbler.

Immune defence, extra–pair paternity, and sexual selection in birds

Secondary sexual characters have been suggested to reliably reflect the ability of individuals to resist debilitating parasites, and females may gain direct or indirect fitness benefits from preferring the most extravagantly ornamented males. Extra–pair paternity provides an estimate of an important component of sexual selection in birds. Species with a high frequency of extra–pair paternity have a variance in realized reproductive success that is greater than the variance in apparent reproductive success, and extra–pair copulations and hence extra–pair paternity by females are often directly associated with the expression of male secondary sexual characters. If sexually dichromatic species have experienced a long period of antagonistic coevolution with their parasites, such species should have evolved larger immune defence organs than sexually monochromatic species. Bird species with sexual dichromatism had larger spleens for their body size than monochromatic species in a comparative analysis. Furthermore, species with a high frequency of extra–pair paternity were sexually dichromatic and had large spleens for their body size. These results are consistent with the hypothesis that females of dichromatic bird species seek extra–pair copulations to obtain indirect fitness benefits in terms of superior resistance of their offspring to virulent parasites.

The Evolution of Mate Choice Copying by Indirect Selection

A two-locus, two-allele population genetic model is used to study whether an allele for mate choice copying can become fixed in a population when it has no direct fitness benefit and there is therefore no cost due to choice. All females have an intrinsic preference for males with a certain trait. If they have the copying allele, they modify this preference on the basis of observations of an older cohort's mating patterns. Our specific model suggests a general rule: copying alleles spread when copying causes females to mate males that have higher total lifetime fitness. It is therefore possible for copying to evolve both when females have preexisting preferences for high-viability males (good genes) and when females are copying a preference for a trait that impairs male survival. Copying can spread through the force of indirect selection even when there is mild direct selection against the copying allele.

Reproductive Sharing in Different Types of Kin Associations

Reproductive Sharing in Different Types of Kin Associations

Female mating preference for bold males in the guppy, Poecilia reticulata.

Although females prefer to mate with brightly colored males in numerous species, the benefits accruing to such females are virtually unknown. According to one hypothesis of sexual selection theory, if the expression of costly preferred traits in males (such as conspicuous colors) is proportional to the male's overall quality or reveals his quality, a well-developed trait should indicate good condition and/or viability for example. A female choosing such a male would therefore stand to gain direct or indirect fitness benefits, or both. Among potential phenotypic indicators of an individual's quality are the amount and brightness of its carotenoid-based colors and its boldness, as measured by its willingness to risk approaching predators without being killed. Here, we show experimentally that in the Trinidadian guppy (Poecilia reticulata) the visual conspicuousness of the color pattern of males correlates positively with boldness toward, and with escape distance from, a cichlid fish predator. Bold individuals are thus more informed about nearby predators and more likely to survive encounters with them. Mate-choice experiments showed that females prefer colorful males as mates, but prefer bolder males irrespective of their coloration when given the opportunity to observe their behavior toward a potential fish predator. By preferentially mating with colorful males, female guppies are thus choosing on average, relatively bold, and perhaps more viable, individuals. In doing so, and to the extent that viability is heritable, they potentially gain indirect fitness benefits by producing more viable offspring than otherwise.

Kin discrimination in salmonids

The data presented here suggest that significant selection pressures towards kin discrimination behaviour patterns result from kin-biased territorial defence behaviour patterns. Salmonids employ a phenotype matching recognition mechanism allowing individuals to discriminate unfamiliar kin. Kin discrimination abilities allow individuals to reduce the levels of aggression associated with territorial defence towards related conspecifics and to defend smaller territories near kin versus non-kin. This kin-biased territorial defence behaviour is observed in at least one species under a wide range of territorial quality conditions. Within kin groups, subordinate individuals obtain a greater number of foraging attempts, resulting in kin-biased foraging within the social group. As a result of this kin-bias, individuals within kin groups show significantly higher mean weight increases (increased direct fitness benefits) and reduced variance in these increases (increased indirect benefits). Since all individuals within the kin groups obtained higher, less variable weight increases, we can argue that individuals are increasing their inclusive fitness as a result of these kin-biased behaviour patterns.

Fitness consequences of helping behavior in the western bluebird

We examined the fitness consequences of helping behavior in the western bluebird (Sialia mexicand) at Hastings Reservation in Carmel Valley, California, USA, and tested hypodieses for how helpers benefit from engaging in alloparental behavior. Both juvenile and adult western bluebirds occasionally help at the nest. During a 12 year period, all adult helpers and most juvenile helpers were male. Helpers usually fed at nests of both their parents and rarely helped when only one parent was present. The frequency of pairs with adult helpers was only 7%, but nearly one-third of adult males helped among those with both parents on the study area. At least 28% were breeders whose nests failed. The propensity to help appears to depend upon parental survival, male philopatry, and die breeding success of potential helpers. Feeding rates were not increased at nests with juvenile helpers, apparendy because breeding males reduced their feeding rates. In contrast, adult helpers increased die overall rates of food delivery to die nest in spite of a reduction in die number of feeding trips made by both male and female parents. Helpers did not derive any obvious direct fitness benefits from helping, but diey had greater indirect fitness than nonhelpers due to increases in nesding growdi rates and fledging success at dieir parents' nests. Helpers fledged fewer offspring in their first nests dian did nonhelpers, suggesting diat they were birds widi reduced reproductive potential. Aldiough we have not yet measured the effect of extrapair fertilizations on die fitness benefits of helping, we calculated die difference in fitness between helpers and nonhelpers as a function of die potential helper's paternity when breeding independendy and his fadier's paternity in die nest at which he might help. In conjunction with constraints on breeding and indirect fitness benefits, we predict that relatedness of males to die young in dieir own as well as dieir parents' nests will influence helping behavior in western bluebirds.

Breast asymmetry, sexual selection, and human reproductive success

Breasts of human females are large compared to those of closely related primate species, and they can thus be hypothesized recently or currently to have been subject to directional sexual selection. Here we show that (1) large breasts have higher levels of fluctuating asymmetry than small breasts, (2) breast fluctuating asymmetry is higher in women without children than in women with at least one child, (3) breast fluctuating symmetry is a reliable predictor of age-independent fecundity, and (4) breast fluctuating symmetry appears to be associated with sexual selection. These conclusions were similar in studies from two cultures differing in fecundity and breastfeeding traditions (Spain; New Mexico, U.S.A.). Choosy males that prefer females with symmetrical breasts may experience a direct fitness benefit in terms of increased fecundity and an indirect benefit in terms of attractive or fecund daughters.