Primary sex ratios in zebra finches: no evidence for adaptive manipulation in wild and semi-domesticated populations.

When breeding diet is restricted, domesticated zebra finches,Taeniopygia guttata, produce male-biased primary and secondary sex ratios, but unexpectedly produce unbiased ratios when food is unrestricted. We investigated the primary sex ratios (at laying) of wild zebra finches in southeastern Australia in response to food supplementation and environmental factors predicted to enhance female breeding condition and to bias the primary sex ratio towards daughters. Molecular sexing of all nestlings in 54 complete broods where every egg hatched, failed to show any significant biases from random. Time of egg laying (month, season) and environmental conditions (rainfall, temperature) did not significantly predict variation in the primary sex ratio, but time of breeding did affect clutch size. Wild zebra finches at our colony did not bias their sex allocation as there were no differences in the primary sex ratio and no differences in the numbers and mass of sons and daughters at the end of parental care (day 35–40 post-hatch). Biases in primary sex ratio of our wild population are probably weak or non-existent possibly due to the unpredictable environment and/or multiple contrary selective forces acting on sex ratios. We also investigated the effects of photoperiod, biases in the adult sex ratio, and parental attractiveness on primary sex ratios of semi-domesticated, laboratory zebra finches. Molecular sexing of three-day old embryos from complete clutches, failed to reveal significant biases from random. In contrast to previous studies, sex of eggs did not correlate with laying order and egg mass declined with order, rather than increased. Domestication may be responsible for these differences.     

Climate and maternal effects modify sex ratios in a weakly dimorphic marsupial

There is growing evidence that the sex ratios of wild vertebrate populations are determined by mechanisms that are directly influenced by environmental characteristics. The Trivers–Willard (TWH) and extrinsic modification (EMH) hypotheses postulate differing determinants of mammalian offspring sex ratios. TWH states that mothers allocate resources according to their current condition and sex-specific offspring costs. EMH states that environmental forces that affect maternal condition determine offspring sex ratios, independently of maternal tactics of sex-biased allocation. We statistically assessed support for each of these hypotheses using long-term life histories of the allied rock-wallaby, Petrogale assimilis; a continuously breeding, polygynous, weakly dimorphic marsupial. We showed that birth sex ratios were equal and independent of maternal and environmental conditions. However, secondary sex ratios were male-biased under good environmental conditions and for high quality mothers or mothers in good condition. Sex differences in offspring survival contributed to these biases: (1) environmental conditions strongly influenced survival to pouch emergence (in support of EMH) and (2) maternal quality affected survival to the end of maternal care (in support of TWH). Environmental effects on survival were more important than maternal factors over the entire period of maternal care and contributed most to male-biased sex ratios at pouch emergence. In contrast, maternal mass was the best predictor of sex ratios at the end of maternal care—the life history stage where offspring body mass differed between the sexes.     

Origin of male-biased sex allocation in orphaned colonies of the termite, <Emphasis Type="Italic">Coptotermes lacteus</Emphasis>

In eusocial insects, sex allocation often constitutes a ground for intracolonial conflicts. This occurrence provides ideal opportunities to test kin-selection theory. A vast literature on this topic is available for social Hymenoptera, but the same field remains almost untouched in termites. A preeminent case is that of some species of Coptotermes, where the sex-allocation ratio in nymphs shifts from near equity to all-male when the primary reproductives are replaced by neotenics. To shed light on the developmental origin of this shift, we compared the sex ratio of the various castes and instars in primary- and neotenic-headed mature colonies of Coptotermes lacteus. The male-biased sex allocation in the latter type of colony results from two concurrent events: first, the sex ratio of the youngest instars (larvae) is male-biased by a 3:1 ratio; and second, all female larvae become workers, while a large fraction of the male larvae proceed to the nymphal and alate stages. Colony-founding experiments showed that inbreeding by itself cannot account for the male bias at hatching. We suggest that both genetic factors, due to the reproductive behaviour of neotenics, and environmental factors (colony condition and resource availability) may influence this process. Their exact nature and respective impact have not yet been clarified.     

Dual mechanism of queen influence over sex ratio in the ant Pheidole pallidula

Social Hymenoptera are general models for the study of parent-offspring conflict over sex ratio, because queens and workers frequently have different reproductive optima. The ant Pheidole pallidula shows a split distribution of sex ratios with most of the colonies producing reproductives of a single sex. Sex ratio specialization is tightly associated with the breeding system, with single-queen (monogynous) colonies producing male-biased brood and multiple-queen (polygynous) colonies female-biased brood. Here, we show that this sex specialization is primarily determined by the queens influence over colony sex ratio. Queens from monogynous colonies produce a significantly more male-biased primary sex ratio than queens from polygynous colonies. Moreover, queens from monogynous colonies produce a significantly lower proportion of diploid eggs that develop into queens and this is associated with lower rate of juvenile hormone (JH) production compared to queens from polygynous colonies. These results indicate that queens regulate colony sex ratio in two complementary ways: by determining the proportion of female eggs laid and by hormonally biasing the development of female eggs into either a worker or reproductive form. This is the first time that such a dual system of queen influence over colony sex ratio is identified in an ant.     

Resource supplements cause a change in colony sex-ratio specialization in the mound-building ant, Formica exsecta

We examine the role of food resources on split sex ratios in Formica exsecta. Models of resource-based sex allocation predict that greater resources will cause an increase in the production of reproductive females (gynes) and an increase in overall size of offspring. We experimentally increased food resources for a subset of colonies in a polygynous population with a very male-biased sex ratio. This increase in food availability caused colonies that were male specialists the prior year to switch to female production. Overall, a significantly greater proportion of food-supplemented colonies produced gynes, compared to control colonies. Moreover, food-supplemented colonies produced significantly larger workers and males (but not gynes), compared to those produced by control colonies. There was, however, no significant difference in the numerical productivity of food-supplemented and control colonies. We also measured the natural association between colony sex specialization and proximity to conifers, which typically harbor honeydew-bearing aphids (an important natural food source). In line with the view that resources play an important role for determining sex ratios in social insects, we found that female-producing colonies were significantly closer to conifers than were male-producing colonies.     

The significance of hotspots to lekking topi antelopes (<Emphasis Type="Italic">Damaliscus lunatus</Emphasis>)

Controversy has surrounded the question of why lek-breeding has evolved in certain ungulate species. Can the behavior be explained simply by males mapping onto a female distribution that is determined by factors unrelated to mating? Or are leks created because estrous females distinguish between males and favor males who cluster? Here I address these questions by looking at spatial distribution in lekking topi antelopes (Damaliscus lunatus). Contrary to the predictions of a model assuming male clustering in the zone of maximum female range overlap, territories were highly clustered also within this zone, and lek size correlated positively with population density. In support of models derived from the ideal free distribution of males onto female dispersion, leks were in areas with high female density during the rut. However, models not taking into account both individual variation in male quality and female mate preferences failed to explain the extreme male clumping also within high density areas, which was revealed by a strongly male-biased sex-ratio on leks. Additional support for the female preference-based model came from the finding that estrous females concentrated onto leks. Female preference for clustered males may develop if males initially follow an ideal free distribution of unequal competitors with high quality males slightly clustered at density hotspots; positive feedback between female benefits of preference for clustered males and male benefits of clustering could lead to contraction of the territorial network and lek behavior. Thus only the female preference-based model correctly predicted a negative correlation between male mating rate and resource density.     

Effects of food availability on dispersal and cub sex ratio in the Mednyi Arctic fox

Since the Pleistocene, Arctic foxes, Alopex lagopus, on Mednyi Island in the North Pacific have been isolated in a small area with rich food resources and no other terrestrial carnivores. This situation provides an unusually simple system within which the effect of food dispersion on demography and social organisation was examined. We studied the composition, location and dispersal of 67 Arctic fox groups and mapped their major food resources (seabird colonies) during 1994–2000 on Mednyi. We compared our observations with the predictions of models of sex-ratio determination. Our observations are most consistent with the predictions of Julliard's (2000) model, where mothers are expected to produce more offspring of the most dispersing sex in low-quality habitats, and more offspring of the most philopatric sex in high-quality habitats. The polygynous foxes on Mednyi Island lived where the principal food resources were patchily distributed (present on 11% of the shoreline), and cub survival to dispersal age or reproductive adult was higher in rich (25/45) than in poor (24/79) home ranges. Furthermore, dispersal was strongly sex-biased: most females (60%) remained on their natal ranges, whereas very few males (9%) did so. Significantly more female than male cubs (54 compared with 24) emerged from dens in resource rich ranges, whereas the sex ratio on poor ranges was approximately equal (51 females and 56 males). While our observations are also to some extent consistent with the local resource enhancement (LRE) hypothesis (which predicts a bias towards the sex most likely to cooperate with parents), this does not account for the observed spatial variability.     

Alternative reproductive tactics and the impact of local competition on sex ratios in the ant Hypoponera opacior

The ant Hypoponera opacior exhibits alternative reproductive morphs of males and females associated with distinct sexual behaviours. Our long-term study reports strong seasonality in sexual production with a mating season in early and one in late summer. Winged (alate) reproductives emerge in June, swarm during the monsoon season and establish new colonies independently. In contrast, wingless worker-like (ergatoid) reproductives that appear in late August mate within their natal or adjacent nests and either do not disperse or establish new nests close by. These divergent dispersal patterns allowed us to analyse the impact of local factors on investment strategies by comparing sex allocation between and within the two reproductive events. The optimal sex ratio for ergatoid reproductives should be influenced both by competition for matings between brothers (local mate competition) and rivalry among young locally dispersing queens for workers, nest sites or food (local resource competition). The greater importance of local resource competition was demonstrated both by a male-biased sex ratio for wingless sexuals and a stronger increase in the number of males with total sexual production than for the number of queens. Microsatellite analysis revealed that inter-nest variation in relatedness asymmetry cannot explain split sex ratios in the August generation. Instead, nests with related ergatoid males raised a male-biased sex ratio contrary to the expectations under local mate competition. In conclusion, male bias in wingless H. opacior indicates that local mate competition is less strong than local resource competition among ergatoid queens over the help of workers during nest foundation.     

Dispersal: an alternative mating tactic conditional on sex ratio and body size

Summary Small male milkweed beetles are less successful at obtaining mates than are larger males. Larger males usually win fights and prevent smaller males from obtaining mates and from choosing larger more fecund females as mates. When sex ratios are male-biased, smaller males are particularly likely to experience these mating disadvantages. It follows that smaller males should be especially responsive to their local competitive environment and behave so as to minimize the mating disadvantages of their smaller size. This paper tests the hypothesis that smaller males disperse from host plant patches with male-biased sex ratios and remain in patches with female-biased sex ratios more readily than larger males.Results show both larger and smaller males disperse from patches with male-biased sex ratios more frequently than from patches with femalebiased sex ratios. As predicted, however, small males are more likely to disperse from patches with male-biased sex ratios and remain in patches with female-biased sex ratios than are larger males.The data also show that smaller males dispersing from patches with male-biased sex ratios obtain more matings than non-dispersing males.For milkweed beetles, moving between patches can be viewed as an alternative mating tactic conditional on male body size and local sex ratio.     

Facultative sex ratio manipulation in American kestrels

Summary For animals that are sexually dimorphic in size, the larger sex is expected to be more costly to raise to independence. Manipulating offspring sex ratios may thus be one means by which parents can fine-tune their reproductive effort to resource availability. Parents in poor physical condition or during poor food years should produce more of the cheaper (smaller) sex. We examined the sex ratios of 259 broods of American kestrels (Falco sparverius) between 1988 and 1990 in relation to food abundance (small mammals) and various attributes to the parents. The proportion of males at hatching increased as the food supply declined, and both male and female parents in poor physical condition were more likely to have male-biased broods than those in good condition. The mortality of eggs and young did not appear to be responsible for the biased sex ratios. The sex ratio was independent of the laying date; however, it was correlated with female body size. Small females produced more sons, perhaps because small size is more detrimental for females than males. Offprint requests to: G.R. Bortolotti     

Variations in the birth sex ratio and neonatal mortality in a natural herd of horses

Variations in birth sex ratios and sex differences in juvenile mortality occur in a number of mammalian species, and in many cases have been linked to resource availability. Most of these biases in offspring sex ratios concern polygynous species with pronounced sexual dimorphism, and where females only are philopatric. Data on species with unusual life-history strategies, such as slight sexual dimorphism or dispersal by both sexes, are of particular interest. In this study of a natural herd of horses (Equus caballus) which experienced an eruptive cycle, and therefore a period of nutritional stress, male offspring had higher neonatal mortality rates in nutritionally poor years than in good ones, whereas “year quality” had no effect on the mortality of female offspring; year quality could therefore be used by mares as predictor of sex-specific offspring survival. We show that the environmental conditions that predicted lower survival of males were negatively related to their production: the birth sex ratio the following year was female-biased; and mares were less likely to produce a son when they had produced a son the preceding year. There was no significant effect of mother's parity, age or rank, or the timing of conception or birth on offspring sex ratios. The mechanism leading to biases in the birth sex ratio could have been the loss of male embryos by mares that did not foal. As there was no evidence for selective abortion of male foetuses in females that did foal the next year, it is not necessary to invoke maternal adjustment, though this remains a possibility. Finally, there was a suggestion that male offspring were more costly to raise than females, since mothers that reared a son in poor years tended to experience an increase in the interbirth interval between their two subsequent offspring. Received: 28 December 1996 / Accepted after revision: 27 July 1997     

Litter sex ratios in the golden hamster vary with time of mating and litter size and are not binomially distributed

Summary Pregnancy rates, litter sizes, and litter sex ratios vary strongly with the time in the estrous cycle at which female golden hamsters (Mesocricetus auratus) are mated. Early matings tend to produce relatively high pregnancy rates, large litters, and female-biased sex ratios, while late matings tend to produce low pregnancy rates, small litters, and male-biased sex ratios. Time of mating and litter size are therefore correlated, but each appears to have an independent effect on litter sex ratio: time of mating and sex ratio are positively correlated, holding litter size constant, while litter size and sex ratio are negatively correlated, holding time of mating constant. At each litter size greater than two, the variance of litter sex ratios is less than the binomial variance expected on the hypotheses of independent sampling with a constant probability of producing a male. The main features of the distribution of litter sex ratios can be generated from a causal model in which different probabilities of producing a male apply to early and late conceptions within each litter. The relationship between litter size and mean litter sex ratio is potentially consistent with several different models for the evolution of adaptive sex-ratio variation. Offrint request to: U.W. Huck     

Egg size and laying order in relation to offspring sex in the extreme sexually size dimorphic brown songlark,<Emphasis Type="Italic"> Cinclorhamphus cruralis</Emphasis>

In some bird species, mothers can advantage the offspring of one sex either by elevating them in the laying order to promote earlier hatching or by allocating greater resources to eggs of the preferred sex. In size dimorphic species, the predictions as to which sex should benefit most from such pre-laying adjustments are ambiguous. The smaller sex would benefit from an initial size advantage to help compensate for the faster growth rate of the larger sex. However, an early advantage to offspring of the larger sex might have a greater effect on their lifetime reproductive success than an equivalent advantage to offspring of the smaller sex. We investigated these hypotheses in the polygynous brown songlark, Cinclorhamphus cruralis, which is one of the most sexually size dimorphic birds known. We conducted within-clutch comparisons and found that females hatched from larger eggs and were initially heavier (but not structurally larger) than their brothers. This may afford females an early competitive advantage, as egg volume remained correlated with chick mass until at least 5 days of age. Similarly, we found that hatch order was still positively associated with nestling mass and size when the brood was 10 days of age, but there was no clear relationship between offspring sex and hatching order. During this study, food was plentiful and there were few obvious cases of nestling starvation. When food is limited, we suggest that the greater nutrient reserves of female hatchlings could not only help compensate for their slower growth, but could also give them a survival advantage over their brothers early in the nestling period. Consequently, egg size dimorphism may be an adaptation that facilitates an early shift in brood sex-ratio towards cheaper daughters in conditions of low food availability.     

Operational sex ratio and alternative reproductive behaviours in the European bitterling,<Emphasis Type="Italic"> Rhodeus sericeus</Emphasis>

We investigated the effects of male population density and male-biased operational sex ratio (OSR) with constant and limited resource density on male mating tactics shown by a freshwater fish, the European bitterling, Rhodeus sericeus. This species spawns inside living unionid mussels. Large males defended territories and were aggressive towards conspecifics under equal sex ratios. They also monopolised pair spawnings with females, releasing 98% of all sperm clouds during mating. However, the mating tactic changed at high male density where large males ceased to be territorial and instead competed with groups of smaller males to release sperm when females spawned. Large, medium and small males now obtained 61%, 33%, and 6% of sperm releases respectively, thereby reducing the opportunity for sexual selection by half. Females spawned at equal rates in the two densities of males, despite lower courtship at high density. These results run counter to the usual expectation that an increasingly male-biased OSR should lead to higher variance in male mating success. Instead, the use of alternative reproductive behaviours by males can lead to lower resource competition and mating variance at high male densities.     

Sex allocation and queen-worker conflict in polygynous ants

Summary Sex allocation theory is developed for polygynous eusocial Hymenoptera in which nests recruit their own daughters as new reproductive queens. Such restricted dispersal of females leads to the expectation of male-biased investment ratios. The expectation depends on the parameter q telling what proportion of the total contribution in the gene pool by all new queens is due to those dispersing. Under queen control the expected sex allocation, expressed as the proportion of resources invested in males, is IM =1/(1 + q). Under worker control, IM depends on the relatedness of old queens, on the number of males they have mated with, and on the proportion of males produced by workers. With single mating and no worker reproduction, the approximate predictions for IM are 1/(1 + q) when the nests have many highly related queens, 1/(1 + 2 q) when the old queens are as related as average worker nest mates, and 1/(1 + 3q) when the old queens are not related to each other at all. The observed investment ratios in polygynous ants would, on average, match values of the parameter q between 0.4 and 0.5. Values of q have not been estimated in nature. If q is smaller than 0.4, which may well be true, the observed sex allocation in polygynous ants is in fact more female-biased than predicted by the theory. This indicates that the female bias found in monogynous ants may not be exceptional and could be due to factors other than worker control of sex allocation. Because the value of q is likely to vary among species, testing the predictions of the theory requires thorough single-species studies.     

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     

Operational sex ratio versus gender density as determinants of copulation duration in the walnut fly,Rhagoletis juglandis (Diptera: Tephritidae)

In laboratory and field studies of the walnut fly, Rhagoletis juglandis Cresson (Diptera: Tephritidae), we assessed the effect of operational sex ratio on copulation duration and partitioned the sex ratio effect into component effects due to male density and female density. In our first laboratory experiment, results were clearly consistent with theoretical expectation: increases in male density were associated with significant increases in copulation duration while increases in female density were associated with significant decreases in copulation duration. These component effects yielded a striking composite effect of operational sex ratio (OSR) on copulation duration in which male-biased ratios were associated with low frequencies of short copulations and female-biased ratios were associated with high frequencies of short copulations. Consistent with a priori expectations concerning costs of territorial behavior, the effect of male density on copulation duration was stronger than that of female density. There was no significant interaction between the effects of gender density on copulation duration: each gender density contributed additively to the composite OSR effect on copulation duration. In contrast to the effect of OSR, overall density had little effect. Field data corroborated these findings fully and showed additionally that OSR in the vicinity of fruit tended in nature to be male-biased. In a second laboratory experiment, we measured copulation duration for individuals exposed alternately to male-biased and female-biased ratios. Individual flies consistently copulated for longer in male-biased environments than in female-biased ones. We propose that this plasticity permits individuals to track changes in local sex ratio over space and time and respond appropriately. Received: 15 November 1995/Accepted after revision: 27 April 1996     

Variation in offspring sex ratio among individual Weddell seal (<Emphasis Type="Italic">Leptonychotes weddellii</Emphasis>) females of different quality

The Trivers–Willard model predicts that in polygynous species, superior-quality females will maximize their fitness by producing male offspring. Using a sample of 1,780 Weddell seal (Leptonychotes weddellii) pups recorded over 31 years, we investigated relationships between offspring sex ratio and maternal age, reproductive experience, an index of maternal lifetime reproductive output, and annual environmental variations. We found evidence that females with higher index of lifetime reproductive output were more likely to produce male than female offspring but found only weak evidence that large-scale environmental variations influenced sex ratios. Our results suggest that mothers manipulate offspring sex to maximize their own fitness, and inherent maternal quality may influence offspring sex. These findings support the Trivers–Willard sex-allocation model. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

No evidence for offspring sex-ratio adjustment to social or environmental conditions in cooperatively breeding purple-crowned fairy-wrens

When fitness returns or production costs vary between male and female offspring, selection is expected to favor females that adjust offspring sex ratio accordingly. However, to what extent vertebrates can do so is the subject of ongoing debate. Here, we explore primary sex ratios in 125 broods of cooperatively breeding purple-crowned fairy-wrens Malurus coronatus. We expected that females might adjust offspring sex ratio because this passerine species experiences considerable variation in social and environmental conditions. (1) However, although helpers substantially increase parental fitness, females (particularly in pairs and small groups) did not overproduce philopatric males (helper-repayment hypothesis). (2) Sex-ratio adjustment based on competition among individuals (helper-competition hypothesis) did not conceal helper-repayment effects or drive sex allocation on its own: while high-quality territories can accommodate more birds, brood sex ratios were independent of territory quality, alone or in interaction with group size. (3) Additionally, males are larger than females and are possibly more costly to produce (costly sex hypothesis), and (4) female offspring may benefit more from long-term effects of favorable conditions early in life (Trivers–Willard hypothesis). Nonetheless, large seasonal variation in food abundance was not associated with a consistent skew in primary sex ratios. Thus, overall, our results did not support the main hypotheses of adaptive sex-ratio adjustment in M. coronatus. We discuss that long-term differential costs and benefits may be insufficient to drive evolution of primary sex-ratio manipulation by M. coronatus females. More investigation is therefore needed to determine the general required sex differences in long-term fitness returns for mechanisms of primary sex-ratio manipulation to evolve.     

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