Evidence for maternally inherited factors favouring male homosexuality and promoting female fecundity

The Darwinian paradox of male homosexuality in humans is examined, i.e. if male homosexuality has a genetic component and homosexuals reproduce less than heterosexuals, then why is this trait maintained in the population? In a sample of 98 homosexual and 100 heterosexual men and their relatives (a total of over 4600 individuals), we found that female maternal relatives of homosexuals have higher fecundity than female maternal relatives of heterosexuals and that this difference is not found in female paternal relatives. The study confirms previous reports, in particular that homosexuals have more maternal than paternal male homosexual relatives, that homosexual males are more often later-born than first-born and that they have more older brothers than older sisters. We discuss the findings and their implications for current research on male homosexuality.     

Sexually antagonistic selection in human male homosexuality

Several lines of evidence indicate the existence of genetic factors influencing male homosexuality and bisexuality. In spite of its relatively low frequency, the stable permanence in all human populations of this apparently detrimental trait constitutes a puzzling 'Darwinian paradox'. Furthermore, several studies have pointed out relevant asymmetries in the distribution of both male homosexuality and of female fecundity in the parental lines of homosexual vs. heterosexual males. A number of hypotheses have attempted to give an evolutionary explanation for the long-standing persistence of this trait, and for its asymmetric distribution in family lines; however a satisfactory understanding of the population genetics of male homosexuality is lacking at present. We perform a systematic mathematical analysis of the propagation and equilibrium of the putative genetic factors for male homosexuality in the population, based on the selection equation for one or two diallelic loci and Bayesian statistics for pedigree investigation. We show that only the two-locus genetic model with at least one locus on the X chromosome, and in which gene expression is sexually antagonistic (increasing female fitness but decreasing male fitness), accounts for all known empirical data. Our results help clarify the basic evolutionary dynamics of male homosexuality, establishing this as a clearly ascertained sexually antagonistic human trait.     

Fecundity of Paternal and Maternal Non-Parental Female Relatives of Homosexual and Heterosexual Men

A variety of social, developmental, biological and genetic factors influence sexual orientation in males. Thus, several hypotheses have attempted to explain the sustenance of genetic factors that influence male homosexuality, despite decreased fecundity within the homosexuals. Kin selection, the existence of maternal effects and two forms of balancing selection, sexually antagonistic selection and overdominance, have been proposed as compensatory mechanisms for reduced homosexual fecundity. Here, we suggest that the empirical support for kin selection and maternal effects cannot account for the low universal frequency and stability of the distribution of homosexuals. To identify the responsible compensatory mechanism, we analyzed fecundity in 2,100 European female relatives, i.e., aunts and grandmothers, of either homosexual or heterosexual probands who were matched in terms of age, culture and sampling strategy. Female relatives were chosen to avoid the sampling bias of the fraternal birth order effect, which occurs when indirectly sampling mothers though their homosexual sons. We observed that the maternal aunts and grandmothers of homosexual probands were significantly more fecund compared with the maternal aunts and maternal grandmothers of the heterosexual probands. No difference in fecundity was observed in the paternal female lines (grandmothers or aunts) from either of the two proband groups. Moreover, due to the selective increase in maternal female fecundity, the total female fecundity was significantly higher in homosexual than heterosexual probands, thus compensating for the reduced fecundity of homosexuals. Altogether, these data support an X-linked multi-locus sexually antagonistic hypothesis rather than an autosomal multi-locus overdominance hypothesis.     

Homosexual incest avoidance among females in captive Japanese macaques

This paper reports a systematic pattern of homosexual incest avoidance among females in a captive group of Japanese macaques (Macaca fuscata) culled from the Arashiyama-West troop known for its high rates of female homosexuality. The study group included three matrilines and two generations. Between eight and 11 females were sexually active over four consecutive mating seasons, and all engaged in both heterosexual and homosexual activity. While all females performed homosexual acts with almost all possible non-kin partners, they systematically avoided homosexual interactions with their mother, daughters, and sisters. This pattern could not be explained either in terms of kin not being simultaneously in estrus, kin avoiding affiliative interactions in general, or non-kin utilizing the tension-reducing effect of estrus to affiliate exclusively with each other. In contrast to homosexual females, heterosexual pairs of relatives (brother-sister, mother-son) were sometimes incestuous. Assuming that female homosexuality expresses the reproductive strategy of females unconstrained by male influence, the present results point to the strong tendency of females to avoid incest and suggest that males are primarily responsible for the reported exceptions to incest avoidance.     

A new group-selection model for the evolution of homosexuality

Abstract. Scientists have long puzzled over how homosexual orientation has evolved, given the assumed low relative fitness of homosexual individuals compared to heterosexual individuals. A number of theoretical models for the evolution of homosexuality have been postulated including balance polymorphism, "Fertile females", hypervariability of DNA sequences, kin selection, and "parental manipulation". In this paper, I propose a new group-selection model for the evolution of homosexuality which offers two advantages over existing models: (1) its non-assumption of genetic determinism, and (2) its lack of dependency on an inefficient altruism relation and family dynamics theory.     

Population size, female fecundity, and sex ratio variation in gynodioecious Plantago maritima

Theory predicts that the sex ratio of gynodioecious populations (in which hermaphrodites and females coexist) will be affected by the relative female fitness of females and hermaphrodites, and by founder events and genetic drift in small populations. We documented the sex ratio and size of 104 populations of the gynodioecious, perennial herb Plantago maritima in four archipelagos in eastern Sweden and western Finland (from latitude 53 to 64 degrees N). The sex ratio varied significantly both among and within archipelagos (range 0-70% females, median 6.3% females). The frequency of females was highest in the northernmost archipelago and lowest in the southernmost archipelago. As predicted, females were more frequently missing from small than from large populations, and the variance in sex ratio increased with decreasing population size. The relative fecundity of female plants (mean seed output per female/mean seed output per hermaphrodite) ranged from 0.43 to 2.16 (median 1.01, n = 12 populations). Among the 12 populations sampled for seed production (four in each of three archipelagos), the frequency of females was positively related to relative fecundity of females and negatively related to population size. The results suggest that the local sex ratio is influenced both by the relative fecundity of females and hermaphrodites and by stochastic processes in small populations.     

Lifetime fitness and age‐related female ornament signalling: evidence for survival and fecundity selection in the pied flycatcher

Ornaments displayed by females have often been denied evolutionary interest due to their frequently reduced expression relative to males, habitually attributed to a genetic correlation between the sexes. We estimated annual and lifetime reproductive success of female pied flycatchers (Ficedula hypoleuca) and applied capture–mark–recapture models to analyse annual survival rates in relation to the patterns of expression (absence/presence) of an ornament displayed by all males and a fraction of females. Overall, the likelihood of expressing the ornament increased nonlinearly with female age and was due to within‐individual variation, not to the selective appearance or disappearance of ornament‐related expression of phenotypes in the population. Accordingly, expressing the forehead patch in a given year did not influence survival probability. However, those females expressing the ornament at early ages (1–2 years old) enjoyed survival advantages throughout lifetime. Although ornamented females had higher lifetime fecundity and fledging success, their yearly reproductive performance, in terms of fledging productivity, decreased as they aged so that, late in life, ornamented females reared fewer offspring than nonexpressing females of the same age. In addition, both strategies (expressing vs. not expressing the trait) returned similar fitness payoffs in terms of recruited offspring. Our results support the hypothesis that fecundity and survival selection are involved in the displaying of this ‘male’ ornament by females.     

Maintenance of gynodioecy in Wurmbea biglandulosa (Colchicaceae): gender differences in seed production and progeny success

 In gynodioecious species, females contribute genes to future generations only through ovules, and to persist in populations they must have a compensatory advantage compared with hermaphrodites that reproduce via ovules and pollen. This compensation can result from greater fecundity and/or superior success of progeny from females. We examined differences in seed production and progeny success between females and hermaphrodites in the geophyte Wurmbea biglandulosa to explain the maintenance of females. Females produced more ovuliferous flowers and had more ovules per flower than did hermaphrodites but this did not necessarily result in greater fecundity, in part because seed production of females was pollen-limited. Over four years in one population, open-pollinated females produced 1.32 more seeds than open-pollinated hermaphrodites (range 1.09–1.63). In two other populations examined for one year only females produced 1.07 and 0.79 as many seeds as hermaphrodites. Seed production of open-pollinated females and hermaphrodites was only 55% and 73% that of cross-pollinated plants, respectively, indicating that both genders were pollen-limited but females more so than hermaphrodites. Open-pollinated seeds from females were 1.18–1.27 times more likely to germinate than seeds from hermaphrodites. No gender differences existed in seedling growth or survival. Hermaphrodites were self-compatible, but selfed seed set was only 80% that of crossed seed set. Crossed seed set of females and hermaphrodites did not differ. Assuming nuclear control of male sterility, relative female fitness is insufficient to maintain females at their current frequencies of 17%, and substantial female fitness advantages at later life-cycle stages are required. Received May 4, 2001 Accepted February 25, 2002     

SEXUAL SELECTION AND FITNESS VARIATION IN A POPULATION OF SMALLMOUTH BASS,MICROPTERUS DOLOMIEUI (PISCES: CENTRARCHIDAE)

Monogamy is often presumed to constrain mating variance and restrict the action of sexual selection. We examined the reproductive patterns of a monogamous population of smallmouth bass (Micropterus dolomieui), and attempted to identify sources of within-season fitness variation among females and known-age males. Many males did not acquire a nest site, and many territorial males were unsuccessful in acquiring a mate. The likelihood that territorial males mated depended on several aspects of nest sites. Mated males of age three were larger than the average size of age-three males in the population. The mean sizes of age-four and age-five mated males were not different from the average of same-age males in the population. Thus, selection resulting from the acquisition of a mate favored large size among only age-three males. Timing of nest construction and breeding among territorial males was negatively related to male size and did not depend on male age after taking male size into account. Indirect evidence (numbers of eggs deposited in nests) suggests that the timing of spawning among females was also negatively related to female size. Fertility selection favored early reproduction within the season by males of all ages, but large male size was favored among only age-four males. The combined early breeding of fecund females and female mate choice of large males may explain the positive correlation between the size of age-four males and the number of eggs acquired. Despite large differences of female fecundity, however, the variance of relative mate number contributed about two times more than the variance of relative fertility among females to the total variance of relative fitness within each sex.     

Is male homosexuality maintained via kin selection?

We tested the kin selection hypothesis of male homosexuality using questionnaire data in a community sample of homosexual and heterosexual men. Homosexual men were no more likely than heterosexual men to channel resources toward family members. Indeed, heterosexual men tended to give more financial resources to siblings than homosexual men. Furthermore, homosexual men were somewhat more estranged from family members, especially from fathers and oldest siblings.     

Male‐limited secondary sexual trait interacts with environment in determining female fitness

Selection for secondary sexual trait (SST) elaboration may increase intralocus sexual conflict over the optimal values of traits expressed from shared genomes. This conflict can reduce female fitness, and the resulting gender load can be exacerbated by environmental stress, with consequences for a population's ability to adapt to novel environments. However, how the evolution of SSTs interacts with environment in determining female fitness is not well understood. Here, we investigated this question using replicate lines of bulb mites selected for increased or decreased prevalence of a male SST—thickened legs used as weapons. The fitness of females from these lines was measured at a temperature to which the mites were adapted (24°C), as well as at two novel temperatures: 18°C and 28°C. We found the prevalence of the SST interacted with temperature in determining female fecundity. At 28°C, females from populations with high SST prevalence were less fecund than females from populations in which the SST was rare, but the reverse was true at 18°C. Thus, a novel environment does not universally depress female fitness more in populations with a high degree of sexually selected dimorphism. We discuss possible consequences of the interaction we detected for adaptation to novel environments.     

Homosexual behaviour and its longevity cost in females and males of the seed beetle Acanthoscelides obtectus

The level of homosexual behaviour is evaluated in one laboratory population of seed beetle and derived lines selected to reproduce early (E) or late in life (L), where inadvertent selection for either low or high heterosexual activity has been detected. The magnitudes of homosexual interaction, measured as chasing and mounting individuals of the same sex, are estimated over different age classes. These magnitudes are correlated with previously observed levels and patterns of age‐specific variation of heterosexual activity of both sexes in the E and L experimental lines. The results obtained support the perception error hypothesis proposing that a low degree of sexual discrimination is genetically correlated with high sexual activity. The fitness costs of the same‐sex interactions are tested by assessing their effects on longevity. In both sexes, the longevities of homosexual pairs are reduced relative to individually‐housed virgin beetles in both the E and L lines, although homosexual interactions have a more pronounced effect on male survival than on female survival. Although the results obtained suggest that the longevity cost of homosexual interactions can be substantial, this cost is much smaller than the cost of heterosexual interactions.     

Courtship behaviour in Japanese macaques during heterosexual and homosexual consortships

Female Japanese macaques (Macaca fuscata) in the Arashiyama population near Kyoto, Japan, are unusual, in that they exhibit what many would consider to be male-typical sexual characteristics. Specifically, they mount other females within the context of temporary, but exclusive, sexual relationships (i.e., homosexual consortships) and they sometimes exhibit a preference for female sexual partners, even when given the choice of a sexually motivated male alternative. In this study, we examined whether female Japanese macaques also exhibited male-typical patterns of courtship behaviour during homosexual consortships. Data were collected on courtship behaviour during heterosexual and homosexual consortships in free-ranging Japanese macaques from the Arashiyama (Japan) population. We analyzed the occurrence of 12 different courtship behaviours during 3374 heterosexual inter-mount intervals and 1412 homosexual inter-mount intervals. Sex differences between heterosexually consorting males and females existed for only two of the 12 courtship behaviours we investigated: inclined-back presentations and sexual vocalizations. Dominant and subordinate homosexually consorting females were sex-typical in their expression of inclined-back presentations and sexual vocalizations. Consequently, facultative same-sex sexual partner preference, mounting and consortships do not co-occur with male-typical patterns of courtship behaviour in female Japanese macaques.     

Male genotype affects female fitness in a paternally investing species

Male nutrient provisioning is widespread in insects. Females of some species use male-derived nutrients for increased longevity and reproductive output. Despite much research into the consequences of paternal nutrient investment for male and female fitness, the heritability, and therefore the potential of this trait to respond to selection, has rarely been examined. Males of several butterfly species provide the female with nutrients in the spermatophore at mating. Females of the green-veined white butterfly Pieris napi (Lepidoptera: Pieridae) use male donations both for developing eggs (resulting in higher lifetime fecundity of multiply mated females), but also for their somatic maintenance (increasing longevity). Using half-sib, father-son regression and full-sib analyses, I showed that paternal nutrient investment is heritable, both in terms of the absolute but also the relative size of the spermatophore (controlling for body size). Male size and spermatophore size were also genetically correlated. Furthermore, a separate study showed male genotype had a significant effect on female longevity and lifetime fecundity. In contrast, male genotype had no influence on the immediate egg-laying rate of females following mating, suggesting limited scope for male manipulation of immediate female oviposition. These results indicate that females may derive both direct (increased lifetime fecundity and longevity) and indirect (sons with greater reproductive success) fitness benefits from paternal nutrient donations in this species.     

Polyandry promotes enhanced offspring survival in decorated crickets

Although female multiple mating is ubiquitous in insects, its adaptive significance remains poorly understood. Benefits to multiple mating can accrue via direct material benefits, indirect genetic benefits, or both. We investigated the effects of multiple mating in the decorated cricket, Gryllodes sigillatus, by simultaneously varying the number of times that females mated and the number of different males with which they mated, measuring aspects of female fecundity and elements of offspring performance and viability. Multiple matings resulted in enhanced female fitness relative to single matings when females mated with different partners, but not when females mated repeatedly with the same male. Specifically, polyandrous females produced significantly more offspring surviving to reproductive maturity than did monogamous females mating once or mating repeatedly with the same male. These results suggest that the benefit females gain from multiple mating is influenced primarily by genetic and not material benefits.     

Schistosoma mansoni: Adult worm chemoattraction,with and without barriers

Heterosexual and homosexual chemoattraction studies were done with 8- to 12-week-old Schistosoma mansoni adults in linear chambers containing Earle's saline, in the absence and presence of both perforated and unperforated dialysis sac chimney barriers. In the absence of barriers attraction was seen in all heterosexual and homosexual combinations. After 90 min of observation at 37 C, organisms maintained at 4 or 37 C for at least 1 hr prior to the assay showed heterosexual attraction similar to those used immediately after perfusion. There was significantly more heterosexual attraction between worms from same than different pairs. In the presence of perforated barriers the greatest attraction was heterosexual, with males moving toward females; heterosexual attraction with females moving toward males was approximately equal to homosexual female attraction, and male homosexual attraction was not seen. In the presence of unperforated barriers the greatest attraction of females toward males occurred during the first 0.5 hr; within 3 to 4 hr females were no longer significantly attracted to males. However, after 0.5 hr males were more significantly attracted to females in unperforated than perforated chimneys. These studies demonstrate that adult schistosomes attract each other in vitro, and that there is a chemical basis for this attraction.     

Sexual selection when the female directly benefits

Why do females of many species mate with males on the basis of traits apparently detrimental to male survival? The answer may lie in the fact that these male traits are correlated with male condition. We consider the argument that high male condition directly benefits female fecundity and/or viability (e.g. through lower transmission of parasites, improved control of resources, or better paternal care). Using a quantitative genetic model we show how female preferences for male traits that indicate condition can evolve, even if the male traits themselves have deleterious effects on both the male and the female's fecundity. So-called ‘arbitrary preferences’ can spread in this way because male traits subject to sexual selection are often under additional selection to become correlated with condition. At equilibrium the positive effects of male condition on a female's fecundity and the negative effects of the male trait on her fecundity are balanced and the female preference is under stabilizing selection. The male trait will often be correlated with viability, but not with fecundity, even though the preference evolved as a result of differences in male fecundity. The mean fecundity of females is not maximized, and can steadily decline as the male trait and female preference evolve. If the male trait has no direct deleterious effects on female fecundity, as may happen in species with no paternal care, female preferences are under continuous directional selection to increase.     

Modelling the Evolution of Traits in a Two-Sex Population,with an Application to Grandmothering

We present a mathematical simplification for the evolutionary dynamics of a heritable trait within a two-sex population. This trait is assumed to control the timing of sex-specific life-history events, such as the age of sexual maturity and end of female fertility, and each sex has a distinct fitness trade-off associated with the trait. We provide a formula for the fitness landscape of the population and show a natural extension of the result to an arbitrary number of heritable traits. Our method can be viewed as a dynamical systems generalisation of the Price equation to include two sexes, age structure and multiple traits. We use this formula to examine the effect of grandmothering, whereby post-fertile females subsidise their daughter’s fertility by provisioning grandchildren. Grandmothering can drive a shift towards increasingly male-biased mating sex ratios due to a post-fertile life stage in females, while male fertility continues to older ages. Our fitness landscapes show a net increase in fitness for both males and females at longer lifespans, and as a result, we find that grandmothering alone provides an evolutionary trajectory to higher longevities.     

Endocrine Function in Male and Female Homosexuals

Serial assays of hormones and their metabolites are reported in the urine of three male and four female homosexuals. Urinary testosterone levels were abnormally low in the two men who practised exclusive homosexuality and were within the normal range in the third, who had both homosexual and heterosexual relationships. In the women assays were generally performed throughout one menstrual cycle; in three the pattern of hormone excretion was ovulatory in character, while in the fourth evidence for ovulation was equivocal. Levels of testosterone and luteinizing hormone (L.H.) were raised in the female homosexuals, while those for oestrogens, particularly oestrone, were below the range for normal heterosexual subjects during their reproductive life; readings of follicle-stimulating hormone (F.S.H.) and pregnanediol were normal in three women. The data reported here are in keeping with the view that abnormalities in endocrine function may occur in both male and female homosexuals.     

Diet affects female mating behaviour in a seed‐feeding beetle

In species where males provide nuptial gifts, females can improve their nutritional status and thus increase their fecundity by mating when in need of resources. However, mating can be costly, so females should only mate to acquire resources when the need for resources is large, such as when females are nutritionally‐deprived. Two populations of the seed‐feeding beetle Callosobruchus maculatus, a species that produces relatively large nuptial gifts, are used to test whether female nutritional status affects mating behaviour. Female access to water, sugar and yeast are manipulated and the fitness consequences of these manipulations are examined together with the effects of diet on the propensity of nonvirgin females to mate. Access to water has a small but significant effect on mass loss over time, lifespan and fecundity of females, relative to unfed controls. Access to sugar (dissolved in water) improves female fecundity and lifespan above that of hydrated females but access to yeast has no positive effects on female survival or reproduction. Diet has a large effect on both receptivity of nonvirgin females to a male and how quickly they accept that male. Unfed females are both more likely to mate, and accept a mate more quickly, than females provided access to water, which are more likely to mate and accept a mate more quickly than females provided with sugar. This rank order of behaviours matches the order predicted if females increase their mating rate when nutritionally deprived (i.e. it matches the effect of diet on female fitness). The results obtained also suggest that mate choice may be condition‐dependent: females from one population (Burkina Faso) show a preference for large males when well‐fed but not when unfed, although this result is not found in a second population (South India). It is concluded that nutritionally‐deprived females are more receptive to mates than are well‐fed females, consistent with the hypothesis that females ‘forage’ for nuptial gifts, or at least more willingly accept sperm in exchange for nuptial gifts, when they are nutritionally deprived.