Operational sex ratios and behavioural sex differences in a pipefish population

In the pipefish Syngnathus typhle, only males brood embryos in specially developed brood pouches, supplying oxygen and nutrients. Laboratory studies have shown that this elaborate paternal care has led to sex-role reversal in this species: males limit female reproductive rate, females are the primary competitors for mates and males exercise greater selectivity in accepting mates. In the first field study of this pipefish, we describe mating behaviour in the wild and test the hypothesis that temporal variations in the operational sex ratio (OSR) determine sex differences in mating behaviour. Our study comprised two reproductive seasons of two sequential mating periods each, the latter separated by a lengthy interval of male brooding. During mating periods, females displayed to all males without wandering and males moved about searching for females, without reacting to all females. The OSR was least female-biased (or even male-biased) at the onset of the breeding season, when most pipefish were simultaneously available to mate, but became strikingly female-biased as males' pouches were filled. The OSR remained substantially female-biased during the second mating period, because few males became available to remate at any one time. As hypothesised, female-biased OSRs resulted in more female-female meetings. As well, females were above the eelgrass more often than brooding males, thus exposing themselves to conspecifics and/ or predators. In the second year, males arrived earlier than females on the breeding site and male pregnancies were shorter, because of higher water temperatures, so rematings occurred earlier. Males met more often during that year than the previous one, but male competitive interactions were still not observed. The field results support laboratory studies and demonstrate that behaviours associated with female-female competition are more prominent when the OSR is more female-biased. Correspondence to: A. Vincent     

Biased primary sex ratio in the bushcricket Poecilimon veluchianus,an insect with sex chromosomes

Offspring sex ratio at hatching was examined in the bushcricket Poecilimon veluchianus. Offspring sex ratios varied significantly between females (Fig. 1). Low mortality prior to sex determination established that this heterogeneity was already present in the primary offspring sex ratio. Sperm age and female age had no influence on offspring sex ratio (Fig. 2). Male age at copulation, however, correlated significantly with offspring sex ratio (Fig. 3). There were two types of males: one type produced predominantly daughters when young and an increasing proportion of sons with age. The other type produced, independent of age, 1:1 offspring sex ratios (Fig. 4). The two types of males seem to occur in approximately equal numbers. Sex ratio variation (1) may adaptively compensate for local sex ratio biases caused by sex-specific motility, or (2) it may be adaptive if there is a sex-differential effect of laying date on offspring fitness. Received: 14 March 1996/Accepted after revision: 24 June 1996     

Food or sex—males and females in a sex role reversed pipefish have different interests

In a sex role reversed pipefish, Syngnathus typhle, we found that basic life history allocations were directly influenced by sexual selection. We investigated time allocation to foraging and mating, respectively, in a choice experiment, giving males and females, of small or large body size, a choice between food and a potential partner. We found that males were more interested in foraging than mating, i.e., were more frequently observed in front of the food than in front of the partner, whereas females were more interested in the potential partner. This reflects sexual selection operating differently on the two sexes, as males and females are relatively similar in other life history traits, such as growth, mortality, age of maturity, dispersal, and parental expenditure. Moreover, large individuals allocated more time to mating activities, small to feeding. Individuals more interested in mating compared to food were subsequently more critical when given a choice between a large (high-quality) and a small (low-quality) partner, whereas individuals more interested in food were not selective. These findings are consistent with our predictions: sex-role reversed males can be relatively sure of achieving one or more matings, and should allocate more time to feeding and, hence, to parental investment, growth and/or future reproduction. Females, on the other hand, have more uncertain mating prospects and should allocate time to imminent reproductive activities, thereby foregoing other life history traits such as growth and future egg production. By this, they also sacrifice future fecundity and attractiveness.     

Bi-directional sex change in a coral-dwelling goby

Bi-directional sex change has recently been reported among obligate coral-dwelling gobies of the genus Gobiodon. However, neither the functional role of this pattern of sex change nor the frequency of sex change in either direction in natural populations is known. We investigated the social structure and pattern of sex change of Gobiodon histrio at Lizard Island on the Great Barrier Reef. The social structure of G. histrio within coral colonies usually consisted of a single juvenile or a heterosexual adult pair. The size of adult social groups was not constrained by coral colony size. In contrast to expectations for pair-forming species, G.␣histrio was primarily a protogynous hermaphrodite. All immature G. histrio were females and sex change from female to male occurred readily when two mature females were placed in a coral colony. In addition, male G. histrio were able to change back to females when two mature males were placed in a coral. Sex change from female to male, however, occurred with over twice the frequency of sex change from male to female. Where two males were placed in a coral colony, heterosexual pairs were most frequently re-established by immigration of females from outside the treatment population. This pattern might be predicted if sex change from male to female is more expensive than sex change from female to male for G. histrio. Where sex change is expensive, movement may be favoured over sex change, particularly where coral densities are high and movement among corals incurs little mortality risk. Received: 10 November 1997 / Accepted after revision: 16 May 1998     

Manipulation of sex differences in parental care

Summary In a species with biparental care two parents cooperate to provide the appropriate amount of care for the young. Recent theoretical treatments consider the evolutionarily stable investment strategy. Under most conditions, the parental investment of the two partners should be negatively correlated, with the shortfall of one partner being partially compensated for by the other. Previous experimental manipulations of biparental care have involved removal of one partner, yet the response of a widowed bird may differ from that of a mated bird whose partner is doing less than its fair share of parental care. We present the first data involving subtle manipulations of sex differences in parental care where both partners continue to care for the young. This study involves pairs in a nestbox colony of european starlings (Sturnus vulgaris L.) with all brood sizes manipulated to five chicks. Pairs were randomly assigned to three groups: (i) male parental care reduced; (ii) female parental care reduce; and (iii) control pairs. Parental care was manipulated by attaching small weights to the base of a bird's tail feathers. Regardless of sex, nest visitation rate was reduced in the weighted birds with an incomplete compensatory increase by their unweighted partner. Additional parental duties were also considered, including shifts in prey type delivered to the nest, in both weighted birds and their partners. The shift in diet and the overall lower total visitation rate in experimental nests contributed to slower chick growth and lower chick weights than in control nests. The data accord with models suggesting that equality of invesment in biparental species is evolutionarily stable, but reveal new dimensions of parental response that need to be taken into account in theoretical treatments.     

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     

Precise sex allocation, local mate competition, and sex ratio shifts in the parasitoid wasp Trichogramma pretiosum

We determined the sex, order, and clutch size of eggs laid by the parasitoid wasp, Trichogramma pretiosum Riley, in the eggs of one of its natural hosts, Trichoplusia ni (Hübner). The parasitoid allocated sex non-randomly to hosts in the laboratory with a variance significantly less than that of a binomial (random) distribution, our null model. More clutches of two or more eggs contained a single male egg as the second or third egg laid than would be expected by chance and none contained two or more male eggs. T. pretiosum also increased the sex ratio (% male) of its offspring with increasing foundress numbers by increasing the frequency of male offspring as the second egg in a two-egg clutch allocated to unparasitized hosts and as the single egg allocated to previously parasitized hosts. These results indicate that T. pretiosum allocates the sex of its offspring precisely. Precise sex allocation is favored under local mate competition because it reduces variation in the number of sons per patch thus maximizing the number of inseminated daughters emigrating from the patch. Similar combinations of female and male offspring emerged from T. ni eggs parasitized by T. pretiosum in the field, again with a sex ratio variance less than that expected for a binomial distribution. These results strongly suggest that this parasitoid species manifests local mate competition.     

Synergism between sib-rearing and sex ratio in Hymenoptera

Summary In many bees and wasps, solitary females produce offspring without help from other females. The transition from lone mothers producing offspring to situations in which females often help to rear siblings is an important step in the origins of complex sociality and nonreproductive castes. Recent work on Hymenoptera has stressed the role of sex ratio variation in this transition; when a mother's brood is more female biased than average, older daughters are favored to help rear their younger siblings because they are more closely related to sisters than to their own offspring. Here the direction of causality is from biased sex ratios, which arise by some extrinsic mechanism, to the origins of sib-rearing (eusociality). We present a model in which there is a synergism between sib-rearing and female-biased sex ratios, which may either complement the sex ratio variation idea by increasing the rate at which helping spreads or be an alternative hypothesis about the origins of eusociality. The synergism in our model depends on three conditions. 1) Daughters that help cause more food to be provisioned per offspring, which in turn causes larger offspring. 2) Females gain more than males by being large, which favors mothers with helpers to produce a higher proportion of daughters. 3) A helper's inclusive fitness rises as her mother's brood becomes increasingly female biased because a female helper is more closely related to her sisters than to her brothers. A female helper may also be more closely related to her sisters than to her own offspring, but this particular sibling-offspring relatedness asymmetry is not required by the synergism model. These three conditions create a synergism which favors a rapid transition from solitary (subsocial) to eusocial. Demographic and ecological factors that facilitate the evolution of eusociality reduce the stringency of the relatedness asymmetry condition (3) required by our idea. The synergism model therefore complements factors other than relatedness that may have been important during the evolution of eusociality.     

Adaptive sex allocation by brood reduction in antechinuses

Antechinuses (Dasyuridae: Marsupialia) exhibit dramatic interpopulation variation in the sex ratio at birth, a pattern which has previously been interpreted in terms of both local resource competition and Trivers/Willard effects. However, Antechinus stuartii usually fail to wean all the young that attach to their teats. At least in captivity, this is because they often eat their young. In free-living populations, brood reduction affects sons and daughters differently. Mothers virtually always wean some daughters. The probability that a daughter will be weaned declines with the number of daughters in the pouch. The health or quality of the mother does not affect the number of daughters weaned. By contrast, mothers tend to wean all or none of their sons. A strong correlate of infanticide against sons is senescence. Old mothers rarely invest in sons, and produce low-quality daughters. Mothers suffer a direct cost (mortality during lace lactation) of male-biased litters. Coupled with data on prenatal sex allocation, these results support the conjoint influence of local resource competition and the Trivers-Willard effect. However, they suggest that in populations where females are largely semelparous, the population optimum generated by local resource competition may be unattainable, because of the importance of producing at least one daughter. These observations support recent theoretical claims that the sex ratio at the population level is not easily predicted, but suggest that the diversity of mammalian sex allocation tactics has been underestimated.     

Birth sex ratios in sheep over six lambing seasons

Summary The birth sex ratio of a commercial flock of Suffolk × sheep, Ovis aries, were studied over six consecutive lambing seasons. In all, data from 1820 lambs were recorded and analysed. The overall birth sex ratio was 49.56% male lambs. Significantly more males (56.23%) were born to ewes with single lambs than to ewes with like-sex twins (47.73%). Significantly more female lambs were born to ewes with triplet births (41.79% male). A significant difference in the birth sex ratio was observed between the first and second half of the lambing season, among like-sex pairs of twin lambs. More males were born in the first half (51.43%) and significantly more females (43.59% male) in the second half of the lambing season. The results are discussed with reference to the theory of Trivers and Willard (1973).     

Female-biased sex allocation in peregrine falcons and other raptors

Summary The sex ratios of nestling Falconiformes in which males are smaller than females are often female biased, despite the apparent costs involved in producing very large female offspring. In Australian peregrine falcons, Falco peregrinus, this bias is most pronounced in broods produced early in the season, and the first eggs to be laid are most likely to produce females. Females that lay early are most likely to be successful breeders. Very large chicks tend to occur in female-biased broods. Collectively, these data suggest that females likely to produce large offspring produce daughters. A modified version of the Trivers/Willard hypothesis is suggested to account for this pattern.Offprint requests to: P.D. Olsen at the second address     

Population dynamics, sex ratio and size at sex change in a protandric simultaneous hermaphrodite, the spiny shrimp Exhippolysmata oplophoroides

One of the main goals of sex allocation theory is understanding sex ratio evolution. However, theoretical studies predicting sex ratios in species with unusual sexual systems, such as protandric simultaneous (PS) hermaphroditism, are rare. In PS hermaphrodites, juveniles first develop into functional males that mature into simultaneous hermaphrodites later in life. Here, we report on the sex ratio (males/males + hermaphrodites) in the PS hermaphroditic shrimp Exhippolysmata oplophoroides. A 2-year study demonstrated that hermaphrodites dominated the population in two different bays. This skewed sex ratio may be explained by limited encounter rates among conspecifics. In agreement with this idea, the density of shrimps was extremely low (≤1 shrimp km⁻²) at the two study sites. Size at sex phase change and sex ratios remained relatively stable through time at the two bays. The stability of these parameters might be explained by the rather steady population structure of this species during the study period. A review of sex ratios in PS hermaphroditic shrimps (Lysmata and Exhippolysmata) revealed considerable variation; some species have male- and others hermaphrodite-skewed sex ratios. The conditions explaining inter- and intra-specific sex ratio variation in protandric simultaneous hermaphroditic species remain to be addressed.     

Parentally biased favouritism in relation to offspring sex in zebra finches

Family conflicts over parental care result in offspring attempting to exert control using solicitation behaviours, whilst the parents are potentially able to retaliate through provisioning rules. However, the evolutionary interests of one parent may not necessarily support the evolutionary interests of the other parent, and such conflicts of interest may be expressed in how the two parents allocate the same form of parental care to individual offspring. Theory suggests that such parentally biased favouritism is a universally predicted outcome of evolutionary conflicts of interest, and empirical evidence suggests that parentally biased favouritism occurs in relation to offspring size and solicitation behaviours. However, unequivocal empirical evidence of parentally biased favouritism in relation to offspring sex is absent, due to being strongly confounded by sex differences in size and solicitation behaviours. Here, we present strong evidence for parentally biased favouritism in relation to offspring sex in zebra finches (Taeniopygia guttata), independent of the effects of chick size and begging intensity. Mothers preferentially provisioned sons over daughters, whilst fathers showed no bias, meaning that sons received more food than daughters. Parentally biased favouritism in relation to offspring sex facilitates parental control over evolutionary conflicts of interest and is probably more widespread than previously realised.     

Colony level sex allocation in a polygynous and polydomous ant

The colony-level sex allocation pattern of eusocial Hymenoptera has attracted much attention in recent studies of evolutionary biology. We conducted a theoretical and empirical study on this subject using the dolichoderine ant Technomyrmex albipes. This ant is unusual in having a dispersal polymorphism in both males and females. New colonies are founded by an alate female after mating with one or more alate males in the nuptial flight. In mature colonies, the reproductive role of the foundress queen is taken over by wingless offspring (supplementary reproductives). Mature colonies are extremely polygynous, with many wingless queens reproducing through intea-colonial mating with wingless males (inbreeding), and producing both alate and wingless sexuals. The population sex ratio of wingless sexuals was found to be extremely female-biased, while the population allocation ratio of alates was almost 1:1. This result suggests that there is local mate competition among wingless sexuals. A specific model for this extraordinary life cycle predicted that the asymmetry of regression relatedness (b _f/b _m) will disappear during the first few generations of wingless reproductives after the foundress dies. If colonies begin to produce alates after several wingless generations, this undermines the hypotheses for intercolonial sex ratio variation based on the relatedness asymmetry. We compared the magnitude of variation in sex ratios and other characteristics between two levels (within-colony-inter-nest and between-colony). Although there was considerable within-colony variation in all the examined characteristics, between-colony variances were always larger. This means that allocation is important at the whole-colony level, not that of the nest. There was no apparent correlation between the sex ratio of alates and colony size. Furthermore, partial correlation analysis indicated that neither the number of workers nor investment in alates explained the variation in the sex ratio of alates. The only factor which was significantly correlated with the sex ratio of alates was the sex ratio of wingless sexuals (a positive correlation). We conclude that both the alate and wingless sex ratios may be influenced by a common primary sex ratio at the egg stage, the variance of which may have genetic components. In the wingless sexuals, partial correlation analysis indicated that colony size and the number of workers explained the sex allocation ratio. The number of wingless females was strongly (positively) correlated with the total investment in wingless sexuals, while the number of males showed no such correlation. There is, however, no convincing explanation for the variation in sex allocation ratio of wingless sexuals, because the estimates of investment in wingless males may have a large sampling error. Correspondence to: K. Tsuji     

Parentage and sex allocation in the facultatively polygynous ant Myrmicatahoensis

Most social groups have the potential for reproductive conflict among group members. Within insect societies, reproduction can be divided among multiple fertile individuals, leading to potential conflicts between these individuals over the parentage of sexual offspring. Colonies of the facultatively polygynous ant Myrmicatahoensis contain from one to several mated queens. In this species, female sexuals were produced almost exclusively by one queen. The parentage of male sexuals was more complex. In accordance with predictions based on worker sex-allocation preferences, male-producing colonies tended to have low levels of genetic relatedness (i.e., high queen numbers). Correspondingly, males were often reared from the eggs of two or more queens in the nest. Further, over half of the males produced appeared to be the progeny of fertile workers, not of queens. Overall investment ratios were substantially more male biased than those predicted by genetic relatedness, suggesting hidden costs associated with the production of female sexuals. These costs are likely to include local resource competition among females, most notably when these individuals are adopted by their maternal nest. Received: 3 March 1998 / Accepted after revision: 20 June 1998     

Maternal investment and sex ratio adjustment in American bison calves

Summary Cow-calf behavior was observed in American bison (Bison bison) to determine if mothers invested differentially in sons and daughters. Cows nursed sons significantly longer than they did daughters in their first three months of life. The increased nursing time for sons was not compensated for by increased grazing time by their mothers. Grazing and activity patterns did not differ significantly between sons and daughters. Cows that had sons bred later in the breeding season than nulliparous cows, barren cows, or cows with daughters. Nine yearling sons compared to only two yearling daughters continued to suckle from their mothers for up to 15 months of age. Cows that had sons the previous year were more apt to be barren in the current year than cows that had daughters in the previous year.     

The development of sex differences in ring-tailed lemur feeding ecology

Sex differences in feeding ecology may develop in response to fluctuations in physiological costs to females over their reproductive cycles, or to sexual size dimorphism, or function to minimize feeding competition within a group via resource partitioning. For most mammal species, it is unknown how these factors contribute to sex differences in feeding, or how the development of males and females reflects these intraspecific feeding differences. We show changes in dietary composition, diversity, overlap, and foraging behavior throughout development in ring-tailed lemurs (Lemur catta) and test how the development of sex differences in feeding is related to female costs of reproduction and year-round resource partitioning. Sex differences in dietary composition were only present when females were lactating, but sex differences in other aspects of feeding, including dietary diversity, and relative time spent feeding and foraging, developed at or near the time of weaning. Sex difference in juveniles and subadults, when present, were similar to the differences found in adults. The low year-round dietary overlap and early differences in dietary diversity indicate that some resource partitioning may begin with young individuals and fluctuate throughout development. The major differences between males and females in dietary composition suggest that these larger changes in diet are closely tied to female reproductive state when females must shift their diet to meet energetic and nutritional requirements.     

Relatedness and sex ratio in a primitively eusocial halictine bee

Lasioglossum laevissimum was studied in Calgary, Alberta, where it is eusocial with one worker brood. Estimates of relatedness were obtained among various categories of nestmate based upon four polymorphic enzyme loci, two of which exhibited significant levels of linkage disequilibrium. Relatedness estimates among workers and among reproductive brood females were very close to the expected 0.75 value that obtains when nests are headed by one, singly mated queen. However, relatedness between workers and the reproductive brood females they reared was significantly lower than 0.75. A low frequency of orphaning with subsequent monopolisation of oviposition by one worker brood female in orphaned nests may explain these results. Workers were significantly more and queens significantly less closely related to male reproductives than expected if all males were to have resulted from queen-laid eggs. Orphaning and worker-produced males contribute to this result. The sex investment ratio was 1:2.2 in favour of females, in excellent agreement with the predictions based upon relative relatednesses between workers and reproductive brood males and females. Adaptive intercolony variation in investment ratios was detected: the sex ratio was more heavily female-biased in nests in which the relative relatedness asymmetry between workers and reproductive brood was more female-biased. The study species is the most weakly eusocial hymenopteran for which relatedness estimates and sex ratio data are available. With high relatedness among nestmates and a strongly female-biased sex ratio, this study suggests the importance of indirect fitness contributions in the early stages of social evolution. Correspondence to: L. Packer     

Variable sex ratio among colonies of ants

Summary Small colonies of ants often produce mostly male alates, while large colonies produce mostly female alates. I present a simple model consistent with this pattern in which males that compete for mates are related (Local Mate Competition). The model explains the observed trend even when relatedness among competing males is low, so that there is only a negligible effect on the predicted sex allocation ratio in the population. The reverse trend is expected when there is competition among related females for a limited resource, such as nest sites (Local Resource Competition); small broods are predicted to be mostly female and large broods are predicted to be mostly male.     

Dimorphism and possible sex change in copepods of the family Calanidae

Adult females of 14 of 25 species of the family Calanidae were found to be dimorphic with respect to the number of aesthetases on the first antenna. The trithek morph, in which most antennal segments bear a complement of one aesthetasc and two setae, appears to be the typical female phenotype. The quadrithek morph is less common and, as in males, odd-numbered segments 2b, 3, 5, 7 and 9 carry quadritheks, i.e., two aesthetascs as well as two setae. Segment 21 in the quadrithek female bears an aesthetasc that is absent in the trithek female. Male antennal segments are distinguished from those of trithek and quadrithek females by pronounced morphological differences in aesthetasc shape and size as well as fusion of one or more pairs of antennal segments. The quadrithek morph usually comprised only a small proportion (<10%) of a local population. Quadrithek morphs were found in tropical and subtropical genera (Cosmocalanus and Nannocalanus), broadly ranging genera (Calanoides), as well as in cool-water lineages (Calanus s.s., Calanus s.l. cristatus, C. s.l. plumchrus, C. s.l. propinquus and C. s.l. tonsus). Maximum frequencies of quadrithek morphs (10 to 12%) in Calanus pacificus californicus occurred during the upwelling season from late winter into spring. No indication of sexual or antennal dimorphism was found in CV C. pacificus californicus sexed by examination of gonad and gonaduct. The quadrithek dimorph appears to be the product of sex change by the larger-sized late-juvenile potential male. The evolutionary and ecological significance of this presumptive hypothesis is that the larger-sized potential male reaching adulthood one or more weeks before maturation of genotypic females may increase its reproductive output by sex change in the course of the final molt to mature as a functional female. Given the sex-change hypothesis, morphogenesis of secondary sexual structures would appear to be controlled by androgenic-like secretions from the genital tract, as has been shown in malacostrocans.