Brood sex ratio is dependent on female mating status in polygynous great reed warblers

Females capable of adjusting the sex ratio of their offspring should be more fit than females lacking such an ability. In polygynous birds where breeding success in males is more strongly influenced by body size and/or attractiveness than in females, females might produce more sons when predicting good conditions or when mating with attractive males. Polygynous great reed warbler, Acrocephalusarundinaceus, males direct most of their feeding effort to the primary (first-hatching) nest and in these nests increase their feeding effort in relation to the brood sex ratio (proportion of sons). Therefore, with the expectation of well-nourished sons, we would predict that females which start breeding first within harems might produce more sons than those which start breeding later, and in anticipation of sons with good genes, that females mated to polygynous males might produce more sons than females mated to monogamous males. I took blood samples from hatchlings and determined the sex using DNA markers. The sex ratio of primary (monogamous and polygynous primary) broods is more male-biased (mean 0.58 males, n = 50) than that of secondary (polygynous secondary and tertiary) broods (mean 0.46, n = 25). Moreover, in the secondary broods with the largest clutch (five eggs), in which offspring are most likely to suffer food shortage, the sex ratio was distinctively female biased (mean 0.33, n = 10). In the primary broods, sex ratio was correlated to harem size. The results suggest that great reed warbler females modify the brood sex ratio to produce both well-nourished sons and sons with good genes, but the former effect is probably stronger than the latter factor. Received: 11 March 1998 / Accepted after revision: 23 May 1998     

Parental investment, adult sex ratios, and sexual selection in a socially monogamous seabird

Although most birds are monogamous, theory predicts that greater female parental investment and female-biased adult sex ratios will lower the polygyny threshold. This should result in polygynous mating, unless obligate biparental care or the spatial and temporal distribution of fertilizable females constrains a male’s ability to take advantage of a lowered polygyny threshold. Here we present data on the extent of male sexually dimorphic plumage, adult sex ratios and breeding season synchrony in three populations of a socially monogamous seabird, the brown booby Sula leucogaster. For one of these populations, San Pedro Mártir Island, we also present data on differences in male and female parental investment, mortality and probability of pairing. The extent of plumage dimorphism varied among populations. Sex ratios were female biased in all populations. On San Pedro Mártir Island, parental investment was female biased, females failed more often than males to find a mate, but there was no polygyny. We suggest that on San Pedro Mártir: (1) a period of obligate biparental care coupled with a relatively synchronous breeding season constrained the ability of males to take advantage of a high environmental polygamy potential and (2) the resulting socially monogamous mating system, in combination with the female-biased adult sex ratio, caused females to be limited by the availability of males despite their greater parental investment. Received: 18 November 1999 / Accepted: 24 January 2000     

Intraspecific parasitism and split sex ratios in a monogynous and monandrous ant (Leptothorax nylanderi)

Sex ratios were bimodally distributed in a population of the monogynous and monandrous ant Leptothorax nylanderi during each of 3 study years. The population-wide investment ratios suggested worker control of sex allocation. Nest-level variation in the proportional investment in virgin queens was not affected by the presence or absence of a queen and only slightly by collecting year, but was correlated with nest size, total sexual investment and, unexpectedly, with differences in nestmate relatedness: small, low-investment nests and nests with several worker lineages produced male-biased sex ratios. Colonies containing several worker lineages arise from usurpation of mature colonies by unrelated founding queens and the fusion of unrelated colonies under strong nest site limitation. In contrast to facultatively polygynous and polyandrous species of social insects, where workers can maximize their inclusive fitness by adjusting sex ratios according to the degree of relatedness asymmetry, workers in mixed colonies of L. nylanderi do not benefit from manipulating sex allocation, as here relatedness asymmetries appear to be the same as in homogeneous colonies. Received: 7 December 1999 / Received in revised form: 29 February 2000 / Accepted: 13 March 2000     

Measurement of parental investment and sex allocation in the European beewolf Philanthus triangulum F. (Hymenoptera: Sphecidae)

Fisher’s 1930 theory of sex allocation predicts a population-wide 1:1 ratio of parental investment. We tested this prediction in the European beewolf, a sphecid wasp that hunts for honeybees as larval food. Because the method to quantify parental investment is of crucial importance, we compared the suitability of several different investment measures. Female/male cost ratios were determined from a sample and the total investment in sons and daughters was calculated. In addition, the actual number of prey items for sons and daughters was directly determined by excavating nests and counting the cuticle remains of the prey. Though mortality was high (70%), it had only a weak effect on the estimate of the investment ratio. Based on commonly used measures like fresh and dry weight of emerged adults, the investment ratio did not deviate from Fisher’s prediction of equal investment. However, progeny weight considerably underestimates investment in males and investment in large progeny. Measures that reflect the allocation of resources more directly (amount of provisions, brood cell volume) revealed a significant male bias and thus contradicted Fisher’s theory. Three kinds of explanation are discussed. First, non-adaptive explanations are unlikely. Second, from the spectrum of alternative adaptive theories, only models that assume a non-linear relationship between amount of investment and progeny fitness seem to be relevant for the study species. Third, though the number of prey in a brood cell seems to be a rather good measure of parental investment in European beewolves, some problems in measuring parental investment remain. These problems are of broad significance. Received: 17 June 1999 / Received in revised form: 6 July 1999 / Accepted: 11 July 1999     

Local mate competition and precise sex ratios in Telenomus fariai (Hymenoptera: Scelionidae), a parasitoid of triatomine eggs

Telenomus fariai is a gregarious endoparasitoid of the eggs of several species of Triatominae (Hemiptera) with a high degree of sibmating: males fertilize their sisters inside the host egg before emergence or emerge first and copulate with their sisters as these emerge. Our results show that, when laying alone, T. fariai behaves adaptively, minimizing offspring mortality and conforming to the prediction of local mate competition (LMC) theory by laying a single male, which is sufficient to fertilize all the sisters. When more than one wasp was placed with one host, sex ratios still conformed to LMC predictions but, despite the decreasing number of eggs laid per wasp, clutch size could not be completely adjusted to avoid mortality. This is not surprising, as superparasitism is rare in the field. Offspring production was independent of the contacts between conspecifics but was affected by the number of mothers laying on a single host egg. The sex of the progeny was precisely determined: a female produced one male per clutch when laying on both unparasitized or previously parasitized hosts. On the other hand, a mother produced less daughters when superparasitizing. Under crowded conditions, the number of eggs laid per female wasp and per host decreased as the number of mothers increased. Developmental mortality also increased with the number of T. fariai eggs per host, determining a maximum of approximately 14 emerged adults. Host resources per individual affected male and female adult size with similar intensity, and male adult mortality was slightly higher than that for females. These results, and previous findings, suggest that T. fariai attains Hamiltonian sex ratios by laying one male and a variable number of females, and that the detection of chemical marks left by conspecifics provides information on the number of foundresses sharing a patch. Received: 4 February 2000 / Received in revised form: 19 April 2000 / Accepted: 20 May 2000     

Infanticide by resident males and female counter-strategies in wild Japanese macaques (Macaca fuscata)

Infanticide was observed for the first time in a wild, non-provisioned troop of Japanese macaques on Yakushima Island, Japan. Eight adult resident males attacked unweaned infants in the pre- and early mating season, and one infanticide was observed directly. These attacks were not consistent with the social pathology, side effect of male aggression, cannibalism, or the resource defense hypothesis, but were generally consistent with the sexual-selection hypothesis. First, most male attackers had risen in dominance rank because several high-ranking males had left the troop. Second, in 78% of cases, male attackers had not previously been observed to mate with the mothers of victims. Moreover, analysis of subject animal DNA showed that males did not attack their own offspring. The two mothers who lost their unweaned infants, however, were not subsequently observed to mate. In fact, almost no mating behavior was observed in the troop. This was most likely due to a poor fruiting year. Resumption of mating by females who lost their infants may have been inhibited by an intervening environmental variable which suppressed female reproductive function. These observations contribute to a growing body of evidence which suggests that sexually selected infanticide can occur in seasonally breeding, multi-male, multi-female primate groups. Female Japanese macaques are known to mate with multiple males. We found evidence that female mating with multiple males inhibits contact aggression towards their infants. Adult males attacked infants eight times more often when they had not previously mated with the mother. Received: 2 September 1999 / Received in revised form: 27 April 2000 / Accepted: 3 May 2000     

Group histories and offspring sex ratios in ringtailed lemurs (Lemur catta)

Birth sex ratios were examined for ringtailed lemurs (Lemur catta) at the Duke University Primate Center. This population provides a long-term database of births under a variety of demographic and management conditions, including two semi-freeranging groups between which males transfer freely and females defend stable territorial boundaries. We examined three hypotheses usually considered in studies of primate sex ratio bias. The Trivers-Willard hypothesis predicts that dominant females produce males, local resource competition at the population level (LRC-population) predicts that the dispersing sex (males) will be overproduced in dense populations, and local resource competition among individuals (LRC-individual) predicts that dominant females overproduce the philopatric sex (females). We also examined a fourth hypothesis, local resource enhancement (LRE), which is usually subsumed under LRC-individual in studies of primate sex ratio evolution. LRE predicts that under certain conditions, females will produce the sex that provides later cooperative benefits, such as alliance support for within- or between-group competition. Our data provide support for LRE: females overproduce daughters given prospects of new group formation, either through group fission or threatened expulsion of young mothers. Behavioral data from Duke and also wild populations show that daughters serve mothers as important allies in this context and LRE effects also have been documented in other mammals that experience similar group histories. Nonsignificant trends in the data supported the LRC-population hypothesis, and we suggest that LRC interacts with LRE to explain offspring sex ratios in ringtailed lemurs. Received: 27 August 1999 / Received in revised form: 6 March 2000 / Accepted: 18 March 2000     

Maternal investment in rhesus macaques (Macaca mulatta): reproductive costs and consequences of raising sons

Maternal investment in offspring is expected to vary according to offspring sex when the reproductive success of the progeny is a function of differential levels of parental expenditure. We conducted a longitudinal investigation of rhesus macaques to determine whether variation in male progeny production, measured with both DNA fingerprinting and short tandem repeat marker typing, could be traced back to patterns of maternal investment. Males weigh significantly more than females at birth, despite an absence of sex differences in gestation length. Size dimorphism increases during infancy, with maternal rank associated with son’s, but not daughter’s, weight at the end of the period of maternal investment. Son’s, but not daughter’s, weight at 1 year of age is significantly correlated with adult weight, and male, but not female, weight accounts for a portion of the variance in reproductive success. Variance in annual offspring output was three- to fourfold higher in males than in females. We suggest that energetic costs of rearing sons could be buffered by fetal delivery of testosterone to the mother, which is aromatized to estrogen and fosters fat accumulation during gestation. We conclude that maternal investment is only slightly greater in sons than in daughters, with mothers endowing sons with extra resources because son, but not daughter, mass has ramifications for offspring sirehood. However, male reproductive tactics supersede maternal investment patterns as fundamental regulators of male fitness. Received: 23 July 1999 / Received in revised form: 23 February 2000 / Accepted: 13 March 2000     

Multiple song repertoire characteristics in the willow warbler (Phylloscopus trochilus): correlations with female choice and offspring viability

Male willow warblers have song repertoires which vary in complexity along several dimensions. We examined whether female choice, as measured by date of pairing, was based on these song characteristics in 4 different years. Pairing date was negatively correlated with song repertoire size in 1 year, and with song versatility in another year, but there was no consistent effect of any song characteristic on pairing throughout the years or in the pooled sample. The variable that best explained how soon a male pairs is male arrival date (only males that had settled territories before the first female arrived were considered in the analysis). This correlation is consistently significant in all years. This is most parsimoniously interpreted as females choosing some habitat characteristic in the same way that males do. A small percentage of males (8.3%) attracted and paired with a second female. The likelihood of becoming polygynous was not explained by any measured song characteristic, but it was related to arrival date: early males were more likely to pair with two females. Males with large repertoires fledged more young in their primary nests, and there was a trend for the offspring of these males to have a greater probability of being recruited into the population. In conclusion, the results show that in most years there is no sexual selection by female preference on song characteristics, although the data on reproductive success is consistent with the idea of repertoire size being an indicator of male quality. Received: 4 June 1999 / Received in revised form: 1 December 1999 / Accepted: 31 December 1999     

Mating frequency, colony size, polyethism and sex ratio in fungus-growing ants (Attini)

The mating frequency of queens was estimated for eight attine ant species, Myrmicocrypta ednaella, Apterostigma mayri, Cyphomyrmex costatus, C. rimosus (four lower attines), Trachymyrmex isthmicus, Serico-myrmex amabalis, Acromyrmex octospinosus and Atta colombica (four higher attines), and correlated to colony size, worker polyethism, and sex ratio. Mating frequency was calculated from within-colony relatedness estimated by CAP-PCR DNA fingerprinting. Most queens of lower attines and T. isthmicus mated with only one male, while those of the three higher attines mated with multiple males. Mating frequency was positively correlated with colony size. Polyethism among workers was dependent on worker age in lower attines but on body size in higher attines, suggesting some correlation between mating frequency (i.e., within-colony gene diversity) and caste complexity. The sex ratio was biased toward females in species where the mating frequency equaled one, but toward males in species where the mating frequency was greater than two. Changing in nest site from ground surface to deep underground may have facilitated the evolution of large colony size in Attini, and this may have resulted in the evolution of polyandry (a queen mates with multiple males). With the evolution of polyandry in higher attines, Atta and Acromyrmex in particular have generated high genetic diversity within their colonies and complex social structures. Received: 26 October 1999 / Revised: 25 May 2000 / Accepted: 24 June 2000     

Parental condition, brood sex ratio and differential young survival: an experimental study in gulls (Larus fuscus)

Empirical evidence is growing that the offspring sex ratio in birds can be biased in relation to the body condition of parents during breeding. The sex ratio bias may come about because (1) the actual production of the two sexes may be skewed and/or (2) there may be a sex bias in early nestling mortality contingent on parental condition. By manipulating parental condition and giving them a control brood to rear, thereby eliminating effects operating via the eggs, we examined the extent to which parental condition influences the post-hatching survival of male and female lesser black-backed gulls, Larus fuscus. We found that the pre-fledging survival of male chicks was strongly reduced in all-male broods reared by parents in poor condition. Pre-fledging survival of female chicks was, however, unaffected by parental condition or brood sex composition. Thus, independently of any production biases, sex differences in nestling mortality alone can bias the offspring sex ratio at fledging in relation to the prevailing rearing conditions. In other studies on gulls we have, however, also shown that females in poor condition at laying preferentially produce female eggs. Clearly a bias in fledging sex ratio can occur within the same species due to a combination of differential production and differential post-laying mortality; the latter can involve a differential effect of poor egg quality on male and female offspring, differential effects of brood sex composition on their survival and a difference in the capacity of parents to rear males and females. All of these processes need to be taken into account in attempting to understand offspring sex ratios. Received: 15 February 2000 / Revised: 7 August 2000 / Accepted: 26 August 2000     

Kin recognition in rainbowfish (Melanotaenia eachamensis): sex, sibs and shoaling

Living with relatives can be beneficial to individuals via the evolution of kin-directed altruism, but this is tempered by the increased risk of inbreeding. Therefore, in social species, the ability to recognise relatives can be highly advantageous. This study focuses on kin discrimination in the Lake Eacham rainbowfish, Melanotaenia eachamensis, an endangered freshwater species from north-east Queensland, Australia. First, I examined kin recognition abilities when a combination of both chemical and visual recognition cues was available. When given a choice of shoaling with same-sex groups, females spent significantly longer with full-sibs rather than half-sibs, full-sibs rather than non-relatives and half-sibs rather than non-relatives. Males spent significantly longer shoaling with full-brothers versus half-brothers, but showed no other shoalmate preferences. Second, in the presence of only chemical cues, females did not discriminate among groups of different levels of relatedness, but males showed a non-significant tendency to associate with full-sibs rather than non-relatives. Male shoaling behaviour seemed to be more influenced by factors other than relatedness, e.g. intra-sexual competition. Finally, I found that the shoaling preferences of females changed when exposed to groups of males. Females preferred to associate with non-relatives rather than half-brothers and non-relatives rather than full-brothers. There was no significant difference in the time spent with half-brothers versus full-brothers. Taken together, my results suggest that females have very good kin recognition abilities. They prefer to shoal with female relatives but avoid male relatives, and so are able to balance the benefits of nepotism and the costs of incest. Received: 2 May 2000 / Revised: 26 July 2000 / Accepted: 30 July 2000     

Leg ornamentation and the efficacy of courtship display in four species of wolf spider (Araneae: Lycosidae)

This study used both correlative and experimental video playback methods to test the hypothesis that the secondary sexual traits of male wolf spiders act to increase the efficacy of visual courtship displays. Direct observations of courtship of several lycosid genera and a review of the literature revealed a significant association between ornamentation and visual courtship displays. This suggests that the ornamentation may be playing the role of amplifier for a visual display. To test this hypothesis, male courtship behaviors of four Schizocosa species were experimentally manipulated using video-imaging techniques. Females of species with non-visually displaying, non-ornamented males (Schizocosa duplex and S. uetzi) did not increase in frequency of receptivity when tufts were added to conspecific males. In a species with a visual display and foreleg pigmentation (S. stridulans), the addition of foreleg tufts increased female receptivity. In a tufted species (S. crassipes), females tended to decrease their receptivity when male ornamentation was completely removed. In visually displaying species, ornamentation acts to increase female receptivity, supporting its role as an amplifier of a visual display. Received: 29 December 1997 / Received in revised form: 23 October 1999 / Accepted: 13 December 1999     

Extra-pair paternity, offspring mortality and offspring sex ratio in the socially monogamous coal tit (Parus ater)

Females of many socially monogamous bird species commonly engage in extra-pair copulations. Assuming that extra-pair males are more attractive than the females’ social partners and that attractiveness has a heritable component, sex allocation theory predicts facultative overproduction of sons among extra-pair offspring (EPO) as sons benefit more than daughters from inheriting their father’s attractiveness traits. Here, we present a large-scale, three-year study on sex ratio variation in a passerine bird, the coal tit (Parus ater). Molecular sexing in combination with paternity analysis revealed no evidence for a male-bias in EPO sex ratios compared to their within-pair maternal half-siblings. Our main conclusion, therefore, is that facultative sex allocation to EPO is absent in the coal tit, in accordance with findings in several other species. Either there is no net selection for a deviation from random sex ratio variation (e.g. because extra-pair mating may serve goals different from striving for ‘attractiveness genes’) or evolutionary constraints preclude the evolution of precise maternal sex ratio adjustment. It is interesting to note that, however, we found broods without EPO as well as broods without mortality to be relatively female-biased compared to broods with EPO and mortality, respectively. We were unable to identify any environmental or parental variable to co-vary with brood sex ratios. There was no significant repeatability of sex ratios in consecutive broods of individual females that would hint at some idiosyncratic maternal sex ratio adjustment. Further research is needed to resolve the biological significance of the correlation between brood sex ratios and extra-pair paternity and mortality incidence, respectively.