Unbiased Sex Ratio Research Articles

Ontogenetic pattern of resource use by the tiny hermit crab Pagurus villosus (PAGURIDAE) from the temperate Chilean coast

The biology of hermit crabs in the temperate zone is understudied in comparison with hermit crabs in the tropics and subtropics. Here we provide the first observations of population traits of the smallest South Pacific hermit crab, Pagurus villosus, using descriptive and experimental approaches. The principal emphasis is on ontogenetic and spatio-temporal variation in the breeding season, recruitment, sex ratio, microhabitat use, and shell occupancy pattern. We also experimentally evaluated colonization rates, in order to assess the pattern of habitat use. P. villosus showed continuous reproduction and recruitment, and an unbiased sex ratio. Algae turf was the microhabitat with highest record of individuals, regardless of their ontogenetic stage. Females were smaller and showed less movement activity on experimental trays than did males, for three microhabitat analyses. Early stages colonized higher proportions of artificial algae and shell hash (only juveniles). Diversity of gastropod shells used by hermit crabs (12 in total) decreased during development, but for all stages Tegula tridentata and Nassarius gayi were the most used. Females in different reproductive conditions (ovigerous and non-ovigerous) showed a shift of shell occupancy pattern likely related to the tradeoff between fitness and shape, weight, thickness and internal volume of shells. Population and life-history traits, i.e., continuous breeding and high resource use during all ontogenetic phases (microhabitats and shells), of P. villosus on the temperate Chilean coast seem more similar to pagurid species from low latitudes. These traits may reflect a tropical origin of this species and/or an adaptive strategy of these tiny crabs in a temperate region.

Sex ratios of juvenile loggerhead sea turtles Caretta caretta in the Mediterranean Sea

Species with environmental sex determination may have sex ratios different from 1:1, and so sex ratio is an important variable in studies on the population dynamics of these species. This is particularly important for the endangered sea turtles, in order to understand the possible effects of human impacts and conservation measures. Unfortunately, only adults show an evident external sexual dimorphism, so that sex ratio data are difficult to obtain and are limited for the juvenile class, which represents the largest part of a population. Here we present the first extensive assessment of sex ratio of juvenile loggerhead turtles (Caretta caretta) in the Mediterranean Sea. A total of 310 dead turtles from four different areas were sexed by direct examination of gonads, the most reliable sexing method. Females were 54.2% of the whole sample, and no significant differences were found between the study areas. However, this value cannot be ascribed to a single population, because specimens from different nesting sites, both within and outside the Mediterranean, share the same foraging areas and each population may potentially contribute with a different sex ratio. Although we found an unbiased sex ratio, when other information from the region about distribution, mixed stocks, and sex ratios are considered, actually present results are compatible with a hypothetical scenario in which a majority of females are produced in the Mediterranean nesting beaches.

Sex ratio variation in the cooperatively breeding alpine marmot Marmota marmota

In cooperatively breeding vertebrate species, a clear theoretical prediction about the direction of sex ratio adjustment can be made: mothers should bias the sex ratio of their offspring towards the helping sex when helpers are absent. A consistent trend in the direction predicted by theory exists in cooperative birds, but theory is still poorly tested in cooperative mammals. Here, multivariate analyses are applied to a long-term data set to test this prediction in two ways in the alpine marmot: (1) across females in a population and (2) in individual females across multiple years. It was shown that in the alpine marmot offspring sex ratio was biased towards the helping sex (males) when helpers were absent, whereas helped mothers produced unbiased sex ratio. Unhelped mothers did not adjust the litter size but produced more sons and fewer daughters than helped mothers. These results support the theoretical prediction and explain well the male bias observed among juvenile alpine marmots at the population level. The occurrence of possible sex ratio manipulations in cooperatively breeding vertebrates is also discussed. Copyright 2004.

Maternal Investment in Captive Giraffes

Sex-biased maternal investment involves differential allocation of resources to production and rearing of sons or daughters as a function of their anticipated reproductive output. We examined reproductive investment among captive giraffes (Giraffa camelopardalis) over a 21-year period to determine extent to which females invest differentially in offspring by sex. We found an unbiased sex ratio at birth and comparable interbirth intervals following rearing of either sons or daughters. Early neonatal mortality compressed interbirth interval and females probably conceived while lactating. We suggest that females invest equally in sons and daughters because males surpass females in size subsequent to the period of infant dependency.

MATERNAL INVESTMENT IN CAPTIVE GIRAFFES

Sex-biased maternal investment involves differential allocation of resources to production and rearing of sons or daughters as a function of their anticipated reproductive output. We examined reproductive investment among captive giraffes (Giraffa camelopardalis) over a 21-year period to determine extent to which females invest differentially in offspring by sex. We found an unbiased sex ratio at birth and comparable interbirth intervals following rearing of either sons or daughters. Early neonatal mortality compressed interbirth interval and females probably conceived while lactating. We suggest that females invest equally in sons and daughters because males surpass females in size subsequent to the period of infant dependency.

Social polymorphism in the sweat bee Lasioglossum (Evylaeus) baleicum (Cockerell) (Hymenoptera, Halictidae) in Hokkaido, northern Japan

The life cycle and social behaviour of the sweat bee Lasioglossum (Evylaeus) baleicum (Cockerell) was investigated in two geographically separate populations in Hokkaido, northern Japan. Colonies were excavated throughout the brood rearing season from an aggregation in Nishioka forest park, Sapporo, and near Kawakita in eastern Hokkaido during 2000 and 2001. The Nishioka population produced two discrete broods during the year and was weakly eusocial; 57% of workers were mated and 28% exhibited some ovarian development, 12–16% of the first brood was male, and workers were on average 4.5% smaller than their respective queen. In contrast, the population at Kawakita was solitary, and produced a single brood per year with an unbiased sex ratio. In addition however, there were some solitary colonies in the Nishioka population and evidence of a partial second brood in some colonies at Kawakita, suggesting differences between the populations are not fixed and that this species is truly socially polymorphic. L. (E.) baleicum is a member of the fulvicorne species group, which includes other examples of social polymorphic species as well as solitary and eusocial species, though this is the only species of this group so far known to exhibit a solitary/non-delayed eusocial polymorphism. Recent studies suggest that social polymorphism has both genetic and environmental influences, raising questions as to the relative import of each.

Low aggression levels and unbiased sex ratios in a prey-rich environment: no evidence of siblicide in Ngorongoro spotted hyenas ( Crocuta crocuta )

Avian models of facultative siblicide predict that rates of sibling aggression and the incidence of siblicide should be lower in prey-rich than prey-poor environments, and that siblicide should only occur when fitness benefits outweigh costs. We tested these predictions by comparing data from spotted hyena (Crocuta crocuta) twin litters in the Ngorongoro Crater, Tanzania, a habitat with a high density of resident prey (176 animals/km2) with similar data from the adjacent Serengeti National Park where density of resident prey is low (3.3 animals/km2). As predicted, rates of sibling aggression in Crater twin litters were substantially lower than those among twin siblings in the Serengeti. There was no evidence of siblicide in the Crater, in contrast to the Serengeti, where facultative siblicide occurs frequently. The growth rate of Crater cubs in singleton litters was similar to that of cubs in twin litters, whereas the growth rate of Serengeti singletons was higher than that of cubs in twin litters. Thus despotic behavior by dominant Crater cubs was unlikely to provide fitness benefits, while dominant Serengeti cubs that eliminated their sibling benefited from increased growth and enhanced survival. Previous studies have demonstrated biases in the sex-composition of hyena litters due to facultative siblicide. No such biases were apparent in Crater litters. Our results provide strong evidence that levels of sibling aggression in spotted hyenas are adjusted in an adaptive manner, and that siblicide is facultative and resource dependent. Our results do not support the idea of pre-natal manipulation of offspring sex by female spotted hyenas in response to changes in resource abundance.

Social biology and sex ratios in the gall-inducing thrips, Oncothrips waterhousei and Oncothrips habrus

We studied the life history and social biology of two haplodiploid eusocial gall-inducing thrips, Oncothrips waterhousei and O. habrus. Both species have alternating generations of non-dispersing, micropteran soldiers and macropteran dispersers. A single female induces a gall, and produces all of the soldiers, which are protogynous and have an overall female-biased sex ratio in both species. The soldiers sibmate and collectively produce about 80% and 50% of the dispersing generation in O. waterhousei and O. habrus, respectively. On a per capita basis soldiers produce about 0.47 and 0.15 the number of dispersers of the foundress in O. waterhousei and O. habrus, respectively. The dispersers have an unbiased sex ratio in both species, but sibmating and local mate competition between soldiers suggests that these sex ratios are not a result of panmictic conditions. A comparison of the proportion of the gall occupied by brood in O. waterhousei and another eusocial galling thrips, Kladothrips hamiltoni, suggests that local resource competition is higher in K. hamiltoni, which might partly explain the lack of sex ratio bias in soldiers of the latter species.

Reproductive division of labour coevolves with gall size in Australian thrips with soldiers.

An analysis of multiple species of Australian gall-inducing thrips with soldiers reveals a significant negative correlation between the size of gall produced and the reproductive division of labour. This correlation suggests that the evolution of smaller galls limited the available space and feeding sites for the offspring of female soldiers, and was a major factor that led to the evolution of an altruistic caste in the gall-inducers. We argue that high levels of inbreeding by singly mated foundresses and incestuous mating by her soldier offspring are key to this evolutionary relationship because they make the relatedness of a female soldier to her daughters and sisters approximately equal. Evidence that relatedness plays an important role is strengthened by the observation of outbred multiply mated foundresses and unbiased sex ratio of dispersers in Oncothrips waterhousei, and the inference that both gall volume and skew decreased along this lineage.

Experimental observations on the sex ratio of adult Schistosoma mansoni, with comments on the natural male bias.

The sex ratio of adult worms has been observed biased towards males in Schistosoma mansoni under natural conditions. The origin of this bias is unknown. This paper determines whether males are more infective than females under controlled experimental bisexual conditions, and hence if the sex ratio is male-biased as a consequence of this. The male and female cercarial infectivities in uni- and bisexual vertebrate host infections using a range of controlled cercarial sex ratios were studied. The results showed that, in experimental unisexual infections, male cercariae were more infective than females, and that in experimental bisexual infections, male cercarial infectivity was similar to that of female, irrespective of cercarial sex ratio. Furthermore, cumulative male and female cercarial infectivity was maximal when sex ratio was equilibrated. The unbiased sex ratios obtained in our experimental bisexual infections are discussed in terms of behavioural and/or biochemical male female interaction. Alternative explanations of the natural biased sex ratio are proposed.

Latitudinal variation in the reproductive biology of the burrowing ghost shrimp Callianassa filholi (Decapoda: Thalassinidea)

Population structure and reproductive ecology of the burrowing ghost shrimp Callianassa filholi Milne-Edwards, 1878 were studied in populations along a latitudinal gradient throughout New Zealand during the breeding season. Size-frequency distributions revealed unimodal populations, with predominantly sexually mature shrimp. All populations showed an unbiased sex-ratio, and there appeared to be no significant difference in size (carapace length, CL) between sexes. At the same time, CL and size at maturity differed significantly between populations; however, a general increase in sizes from north to south was not consistent throughout the latitudinal range studied. The timing of the breeding cycle differed significantly between populations, and breeding started earlier in southern populations. Number of embryos (fecundity) increased linearly with female CL at each location, but rates differed significantly between populations. Embryo size was not related to number of embryos, and the former increased significantly with latitude. With the exception of embryo size, observed differences in body size/size at maturity and reproductive timing between C. filholi populations are thought to be determined by food availability rather than temperature. Thus, further study is suggested on these aspects of thalassinid reproductive biology.

Comparison of development and reproduction in offspring produced by females of Phytoseiulus persimilis Athias-Henriot (Acari : Phytoseiidae) under two prey conditions

Females of Phytoseiulus persimilis deposit eggs with a female-biased sex ratio under an ample prey condition, but deposit smaller eggs with an unbiased sex ratio under a poor prey condition ; in this condition male eggs and female eggs are produced alternately. The relationship between the size of the eggs and the life history characteristics of the immature and adult stages was examined by rearing two different sized eggs, which are laid under the ample and poor prey conditions, to clarify the changes in sex ratio and the alternate production of sexes. Female offspring produced under the poor prey condition developed more slowly than those produced under the ample prey condition did, and the former consumed fewer prey eggs daily during the nymphal stage. However, the total prey consumption during the entire nymphal stage and the body size of adult offspring showed no differences between the two prey conditions. In addition, females from both conditions had similar reproductive abilities. Male offspring showed the same trend in developmental and preyconsumption rates, whereas adult males from the poor prey condition showed a lower fertilization potential than those from the ample prey condition. The decreases in the developmental rates of both sexes and in the reproductive abilities in males are disadvantageous characteristics, but the alternate production of sexes may compensate and assure female offspring of insemination even under the poor prey condition.

Effect of prey density on sex ratio of two predacious mites, Phytoseiulus persimilis and Amblyseius womersleyi (Acari: Phytoseiidae)

The sex ratios of two phytoseiid mites, Phytoseiulus persimilis and Amblyseius womersleyi, were observed under various prey conditions. Upon consumption of abundant prey, both phytoseiids produced progeny in a female-biased sex ratio (approximately 0.8 females). When few prey were consumed, the sex ratio was lowered to 0.5 (the unbiased sex ratio). Under the conditions in which the unbiased sex ratio was observed, male and female progeny appeared in an alternating sequence. To determine the change in the sex ratio and the sequence of progeny, the size of eggs deposited by females under various prey conditions was first compared. Survivorship and developmental rate of progeny (immatures) hatched under ample and poor prey conditions were also examined. The eggs deposited under poor prey conditions were smaller than those deposited under ample prey conditions. This is an indication that the phytoseiid females did not invest extra energy into the eggs to secure survival of their progeny under poor prey conditions. The male and female progeny from the small eggs developed slowly, probably due to the small egg size. However, hatchability of the small eggs and survival of the immatures were the same as those of the normal eggs when the immatures were reared under ample prey conditions. The immature survivorship was little affected by the prey consumption rate of their mothers when the immatures were reared under poor prey conditions. We concluded that the sex ratio of phytoseiid mites is not determined by the characteristics of the progeny, but by the nutritious condition of the females.

Biased sex ratios and parasite mating probabilities.

SummaryAn earlier paper (May, 1977) developed a theoretical framework for exploring the consequences of dioecy for the population dynamics of schistosomes, assuming an unbiased sex ratio. This paper extends the analysis to biased sex ratios, as have been reported in practice. We consider the relationships of the mean number and distribution of worms among hosts, the sex ratio, and the mating system (monogamous or polygamous) to: (i) the female mating probability, Φ the prevalence of mated female worms. Ω: and (iii) the mean number of mated female worms per host, ξ. Among other results, we show how high values of Φ are associated with male-biased sex ratios and polygamous mating; that Ω is independent of the mating system and is relatively unaffected by the sex ratio; and that ξ is maximal for unbiased sex ratios given monogamous mating, and for female-biased sex ratios if mating is polygamous. These results, together with the confounding effects of the mean number and distribution of worms, are described in detail in the main body of the paper.

Allocation of reproductive effort in Mus domesticus: responses of offspring sex ratio and quality to social density and food availability

Female mammals in good condition can maximize their inclusive fitness by investing more in male offspring than in female offspring during periods of poor environmental quality. To test this hypothesis, we measured the effects of undernutrition and crowding before and during gestation on the sex ratio and weight of offspring at parturition and at weaning in Mus domesticus. Sex ratio was not significantly affected by density. Dams altered the sex ratio of their offspring in response to food availability, but only if variance in competitive success within the experimental subpopulation was evident. Thus ad lib fed females produced litters with an unbiased sex ratio, competitively successful females under moderate food availability produced a male-biased sex ratio, and severely food deprived females produced litters with a female-biased sex ratio. In groups that experienced competition for food, successful dams favoured male offspring during lactation. These results are consistent with the predictions of Trivers and Willard (1973). Analysis of within-cell variance and covariance suggests that the interaction of social structure and food availability provides specific cues for the dams' tactical reproductive choices.

Variable sex ratio strategy of Telenomus heliothidis (Hymenoptera: Scelionidae): adaptation to host and conspecific density.

The sex allocation behavior of the solitary egg parasitoid Telenomus heliothidis Ashmead was investigated by examining the response of females reared in isolation and under crowded conditions. Females reared in isolation adjusted their sex ratio with foundress and host number per patch in accordance with the predictions of local mate competition (LMC) theory. However, females did not shift their sex ratio in response to conspecifics foraging on the same host patch or to contact with previously parasitized hosts. Instead, shifts were associated with encounter rate and a sequence of oviposition. Females maintained under crowded conditions responded to host patches much differently. One-day-old females which had lived under crowded conditions for 24 h produced sex ratios similar to those of continuously isolated females. However, females reared under crowded conditions for 7 days consistently produced unbiased sex ratios, and exhibited a different sequence of oviposition. This shift appeared to be due directly to crowding rather than age, oviposition experience or sperm depletion since the effect could be reversed by subsequent isolation.

Some data on the fertility of bank voles (Clethrionomys glareolus britannicus) in the laboratory supporting the hypothesis of induced ovulation

83 (40%) litters with an average of 3.42 pups and unbiased sex ratio were born of 207 couples. Fertility and litter average were higher in summer and autumn. Most females were fertilized on the 1st day spent with a male, which supports the mating-induced ovulation hypothesis. Infantile mortality was highest at birth and during the 1st 5 days of life. 26% of the pups died before weaning (day 25), i.e. an average of 1 per litter.

Group selection is implicated in the evolution of female-biased sex ratios

Female-biased sex ratios are common among arthropods that mate in small groups with episodic dispersal1–3. When breeding groups are founded by more than one female, individual (within-group) selection favours an unbiased (1:1) sex ratio, regardless of group size and degree of inbreeding (or sibmating), and regardless of the intensity of local competition among siblings for mates. On the other hand, female-biased sex ratios are favoured by group selection in randomly structured populations. Existing treatments of the evolution of female-biased sex ratios1,2,4–6 correctly predict the result of evolution, but do not make clear that it is a balance between opposing forces at two levels of selection3. I now show this to be so.