Operational sex ratios and sperm limitation in populations of Drosophila pachea

Males of the cactophilic fruitfly, Drosophila pachea, produce relatively few but very large sperm, and partition their limited gamete numbers among successive mates. The present study found that males take 10 days longer than females, post-eclosion, to become sexually mature. The pattern of testes development suggests that the need to produce testes long enough to manufacture the giant sperm is the cause of the delayed male maturity. These findings generate the prediction that the operational sex ratio (OSR) of populations will be female-biased. The size, sex ratio, and OSR of natural populations were examined. In general, local populations tended to be small and sex ratios tended to be slightly male-biased. However, as predicted, the OSR of populations, at least in one season, tended to be female-biased, with an average of 2.3 receptive females for each sexually active male. Results of laboratory experiments to determine the relationship between female remating frequency and fitness, and between population OSR and productivity, suggest that natural populations with female-biased OSRs are sperm-limited. The origin and maintenance of sperm gigantism and the unusual sperm-partitioning behavior of males are discussed with respect to population structure.     

Apparent resource competition among embryos in the brood pouch of a male pipefish

Embryo success was studied in the paternally brooding pipefish Syngnathus typhle. During brooding, which lasts about a month, males provide embryos in their brood pouch with nutrients and oxygen via a placenta-like structure. Egg size depends on female size. In aquaria, males were mated with differently sized females to give the following treatments: M, mixed-egg-size broods of approximately half large and half small eggs; L, single-egg-size broods of large eggs; S, single-egg-size broods of small eggs; and F, field mated males. All males were kept in aquaria for a full brooding period. For each egg-size category, the number of newborn was compared with the number of eggs the male initially fertilized in his brood pouch. Within mixed-egg-size broods, a higher proportion of large eggs survived and large eggs resulted in heavier newborn than small eggs. Indeed, small eggs from a mixed-egg-size brood had significantly lower relative success (proportion of embryos surviving to birth) than those from a brood entirely composed of small eggs. The implication is that embryos compete for resources within the brood pouch, and that competitive success depends on egg size. Given that females produce eggs corresponding in size to their body size, and that females are known to compete indirectly for access to mates (i.e., the sex-roles are reversed), this intrabrood competition could be seen as an extension of female-female competition, but alternative explanations are discussed. Received: 28 April 1995/Accepted after revision: 28 October 1995     

The costs of male parental care and its evolution in a neotropical frog

Summary Parental care is practiced exclusively by males of the Puerto Rican frog, Eleutherodactylus coqui. Males brood clutches of direct-developing eggs in non-aquatic nest sites and defend eggs against cannibalistic nest intruders. Here, I report on energetic and mating costs incurred by males that provide parental care, and suggest how these proximate costs affect male fitness and the evolution of male parental care in this species. Energetic costs are small for brooding males in comparison to non-brooding, calling males. Brooding males had a higher frequency of empty stomachs and lost small, but significant, fractions of their initial body mass during parental care. Abdominal fat bodies of brooding males during the middle third of parental care were significantly smaller than those of calling males; those of males brooding eggs in earlier or later stages were not different. The mating cost of parental care is greater. Most brooding males cease calling during parental care. However, gravid females are available (i.e., known to mate) on most nights during the principal breeding season; hence non-calling males miss potential opportunities to mate. A mating cost was estimated by calculating nightly mating probabilities for calling males in a plot where nightly calling male densities and daily oviposition schedules were known. On average, a male exhibiting normal calling behavior would be expected to obtain a new mate once every 35.7 days. Hence a brooding male that ceased calling for a 20-day parental care period would miss, on average, 0.56 additional mates. Males that were more successful than average in attracting mates could miss up to 1.63 matings. A marginal value model (Fig. 1) is used to analyze the net effect on male fitness of parental care benefits and costs in E. coqui (Fig. 3). The model indicates that males garner the highest reproductive success by providing care from oviposition through hatching. There is no stage during the pre-hatching period at which a desertion strategy would yield higher reproductive success. In fact, the model suggests that males should provide full parental care even in the face of much higher mating costs than currently obtain in the system.     

The effect of maternal body size on embryo survivorship in the broods of pregnant male pipefish

The occurrence of male pregnancy in the family Syngnathidae (seahorses, pipefishes, and sea dragons) provides an exceptionally fertile system in which to investigate issues related to the evolution of parental care. Here, we take advantage of this unique reproductive system to study the influence of maternal body size on embryo survivorship in the brood pouches of pregnant males of the broad-nosed pipefish, Syngnathus typhle. Males were mated with either two large females, two small females, a large then a small female, or a small then a large female. Our results show that offspring survivorship depends on an interaction between female body size and the number of eggs transferred by the female. Eggs of larger females deposited in large numbers are more likely to result in viable offspring than eggs of smaller females laid in large numbers. However, when females deposited smaller numbers of eggs, the eggs from smaller females were more likely to produce viable offspring compared to those from larger females. We found no evidence that this result was based on mating order, the relative sizes of competing females, or egg characteristics such as dry weight of eggs. Additionally, male body size did not significantly influence the survivorship of offspring during brooding. Our results suggest that the factors underlying offspring survivorship in pipefish may be more complex than previously believed, with multiple factors interacting to determine the fitness of individual offspring within the broods of pregnant males.     

Clutch loss affects the operational sex ratio in the strawberry poison frog Dendrobates pumilio

Both modelling and field data from three breeding seasons show that an environmental factor, clutch loss (CL), affects the operational sex ratio (OSR) and therefore male mating frequency in strawberry poison frogs. Clutch loss affects the length of reproductive cycles of both sexes: with increasing clutch losses, males spend proportionately more time than females in parental investment activities. Because of this, males spend relatively less time in the mating pool, i.e. exhibit proportionately more time-out than females in comparison to a situation with low or no clutch loss. Hence, clutch loss leads to a less male-biased OSR, coupled with a decrease in the opportunity for sexual selection. Furthermore, this study resolves an apparent paradox, the negative correlation between mating frequency and reproductive success (=number of produced tadpoles) of individual males in one breeding season. Clutch loss decouples the correlation between mating frequency and reproductive success because females re-enter the mating pool when they lose their offspring. However, clutch loss diminishes the reproductive output. Similar consequences of clutch loss on the OSR may be true for many species where both sexes reproduce frequently in one breeding season.Communicated by J. Christensen-Dalsgaard     

Experimental assessment of ecological and phenotypic factors affecting male mating success and polyandry in northern watersnakes, Nerodia sipedon

To resolve conflicting field observations regarding the action of sexual selection, we used breeding experiments and paternity analysis of the 927 resulting offspring to assess how male size, condition, tail length, genetic similarity to the female, and variation in operational sex ratio (OSR) affected male reproductive success and the incidence of polyandry in northern watersnakes (Nerodia sipedon). Only size affected male mating success. Large males were more successful, but only when male size varied substantially and competition among males was intense (i.e., male-biased OSR). The conditional nature of the size advantage may explain why studies of free-living watersnakes have produced inconsistent results regarding the relationship between male size and mating success. Size differences between males did not affect the proportion of offspring each male sired within multiply sired litters. We found positive size-assortative mating, but only when the OSR was female biased, suggesting that smaller males had improved access to females when competition among males was reduced, but that competition with larger males still restricted mating opportunities of small males to less preferred, smaller females. Most litters (58%) were multiply sired and larger females were more likely to produce multiply sired litters, similar to free-living watersnakes. There was no association between the incidence of multiple paternity and OSR, however, suggesting that polyandry is not simply a function of opportunity, with females passively waiting for males to court them.     

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     

Reproductive rates,operational sex ratios and mate choice in St. Peter’s fish

Operational sex ratio (OSR) theory predicts that sexual differences in potential reproductive rates (PRRs) create biases in the OSR and thus determine the relative strength of sexual selection (competition and choice) operating on each sex. Although this theory is well accepted, empirical studies that quantify it are still lacking. This paper presents such a study. I measured the natural OSR of Galilee St. Peter’s fish (Sarotherodon galilaeus) in the field (Lake Kinneret) and examined the direction of mate choice in the laboratory. The OSR in Lake Kinneret was male biased. Both a male-biased sex ratio and higher male reproductive rates (twice as fast as females) contributed to the skew in the OSR, but the sexual differences in PRR were shown to be the main factor causing variation in the OSR. Females, the sex with the lower PRR, were more selective for mates. The faster male reproductive rate may explain why females are more selective for mates despite varying less in quality. Received: 29 May 1995/Accepted after revision: 13 April 1996     

Variance in female quality, operational sex ratio and male mate choice in a bushcricket

Male bushcrickets, Kawanaphila nartee, exercise mate choice when nutrients are limited. Male mate choice is associated with a female-biased operational sex ratio (OSR) that arises from an increased relative paternal investment under nutrient limitation. However, increased male choosiness could be attributable to the fact that females vary more in fecundity, and consequently in mate quality, when nutrient limited. Our objective was to experimentally partition the influences of OSR (male or female bias) and variance in mate quality (high or low) and to assess their relative influence on the intensity of mate choice by male bushcrickets. Female quality was manipulated by controlled feeding regimes that directly affected female fecundity. We found that males and females engaged in sexual interactions sooner under a male-biased than a female-biased OSR. Males were more likely to reject females on their first encounter when variance in female quality was high. However, the effect of quality variance on the total number of rejections during a 4-h observation period was dependent on the perceived OSR. A male's prior experience of variance in female quality did not influence male choosiness. Our observed rates of mate rejection conformed well with those predicted from recent theoretical models of sexual differences in choosiness. In conclusion, our results show that the opportunity for selection via male mate choice is influenced by an interaction between OSR and the variance in mate quality that arises within nutrient-limited populations of females. Received: 5 January 1998 / Accepted after revision: 25 October 1998     

The sex in short supply for matings varies over small spatial scales in a katydid (Kawanaphilanartee, Orthoptera: Tettigoniidae)

In katydids such as Kawanaphilanartee, a female bias in the operational sex ratio (OSR) results in female competition for mates and male choice of mates. Previous work showed that the excess of sexually active females occurs when food availability is low, in part because less food increases the propensity of females to mate as they forage for the large edible spermatophores produced by males. In this study with K.nartee, a pollen-feeding species, we estimate natural variation in numbers of sexually active males and females by assessing male calling activity and the propensity of females to respond to experimental calling males. We found an excess of sexually active males at a site with many flowers and an excess of sexually active females at a site with few flowers about 900 m away. Between-site differences in gut masses of calling males were consistent with the hypothesis that pollen availability controls OSR. Finally, at a third site where flowers were at first scarce, we found that the initial excess in sexually active females changed to an excess of sexually active males after a clump of grass-trees flowered. The mean gut mass of all sampled males from this site increased after flowering. The large variation in OSR that we document for K. nartee highlights the importance of identifying the appropriate spatial and temporal scales over which OSRs are measured in studies of factors controlling sexual selection. Received: 13 May 1997 / Accepted after revision: 27 October 1997     

Reproductive success of male bank voles (<Emphasis Type="Italic">Clethrionomys glareolus</Emphasis>): the effect of operational sex ratio and body size

The operational sex ratio (OSR) may influence the intensity of competition for mates and mate choice and is therefore thought to be a major factor predicting the intensity and direction of sexual selection. We studied the opportunity for sexual selection, i.e., the variance in male reproductive success and the direction and intensity of sexual selection on male body mass in bank vole (Clethrionomys glareolus) enclosure populations with experimentally manipulated sex ratios. The opportunity for sexual selection was high among male-biased OSRs and decreased towards female-biased OSRs. Paradoxically, selection for large male body mass was strongest in female-biased OSRs and also considerable at intermediate OSRs, whereas at male-biased OSRs, only a weak relationship between male size and reproductive success was found. Litters in male-biased OSRs were more likely to be sired by multiple males than litters in female-biased OSRs. Our results suggest that the intensity and direction of sexual selection in males differs among different OSRs. Although the direction of sexual selection on male body mass was opposite than predicted, large body mass can be favored by sexual selection. Naturally varying OSRs may therefore contribute to maintain variation in male sexually selected traits.     

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.     

Evidence for seasonal mate limitation in populations of an intertidal amphipod, Corophium volutator (Pallas)

Potential rates of reproduction (PRR) differ between the sexes of many animal species. Adult sex ratios together with PRR are expected to determine the operational sex ratio (OSR) defined as the ratio of fertilizable females to sexually active males at any given time. OSR is expected to determine the degree to which one sex competes for another—the limiting sex. We explored the potential for mate limitation in an intertidal amphipod, Corophium volutator (Pallas). Males have higher PRR than females, but males may be limiting because of extreme female-biased sex ratios observed in this species. Consistent with this idea, late season females were less likely to be ovigerous and had smaller size-specific clutches, both of which were associated with seasonal declines in availability of males of reproductive size. Seasonal changes in ovigery could not be explained by seasonal changes across sites in other factors (e.g., female body size or phenology of breeding). Smaller females were less likely to become ovigerous later in the season at three of four sites. Seasonal reductions in clutch size also occurred among small females expected to be reproducing for their first time. In complimentary laboratory experiments, reduced likelihood of ovigery and reduced fecundity occurred when the number of receptive females was increased relative to availability of a reproductively active male. Our results suggest male mate limitation can occur seasonally in this species and that male limitation is regionally widespread and may affect recruitment.     

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     

Sex ratios and intrasexual competition for mates in a sex-role reversed shorebird,Wilson's phalarope (Phalaropus tricolor)

Summary Operational sex ratio (OSR) was proposed by Emlen and Oring (1977) as an empirical measure of the intensity of sexual selection. Few studies, however, have examined the link between OSR and levels of intrasexual competition, which may influence selection. We studied the seasonal relationship between OSR and female-female competition for mates in Wilson's phalarope (Phalaropus tricolor), a sex-role reversed, non-territorial shorebird. Positive correlations between four measures of OSR (Scan Ratio, Day Ratio, Focal Ratio, and Chase Ratio) indicated seasonal changes in the availability of mates for females. Changes in mate availability resulted from the interaction between paternal care and female emancipation, asynchronous spring arrival schedules of the sexes (Reynolds et al. 1986), and the effect of clutch failure on renesting opportunities. Measures of intrasexual competition (courtship chases, percent males defended, rate and intensity of mate defense, and female-male proximity) varied significantly within and among years. Univariate and multivariate correlations indicated general agreement between measures of OSR and estimates of intrasexual competition. Our results suggest that OSR may provide a useful estimate of the opportunity for sexual selection, especially in species with matedefense mating systems.     

Duration of paternal care in pine engraver beetles: why do larger males care less?

Male pine engravers, Ips pini (Coleoptera: Scolytidae), assist their mates during reproduction by removing the debris that accumulates while females excavate oviposition tunnels in the phloem tissue of host tree bark. Although duration of paternal care and male reproductive success are positively correlated, large males leave their mates and brood sooner than small males. We address two hypotheses to explain the earlier departure of larger males from their breeding galleries: (1) females oviposit most rapidly when paired with large males, thereby reducing the length of time that paternal care increases male reproductive success, (2) larger males have better prospects for future reproduction, and thus leave their galleries in search of new breeding opportunities sooner than smaller males. Contrary to the first hypothesis, when females were paired either with large or small males, there was no effect of male size on their rate of oviposition. Consistent with the second hypothesis, males that initiated breeding galleries were larger than males from the general population. In addition, large males flew farther and faster on flight mills than small males, which may indicate that large males have an advantage in locating suitable breeding sites. Thus, we suggest that large male pine engravers leave their galleries earlier than small males because large individuals have better prospects for future reproduction. Received: 30 November 1997 / Accepted after revision: 23 May 1998     

Parental care sex differences in the brown bullhead,Ictalurus nebulosus (Pisces,Ictaluridae)

Summary Males were the principal care-givers in the brown bullhead, Ictalurus nebulosus. Direct observations on individually tagged adults in nature revealed that males attended broods at closer distances than females and were the most frequent lone care-givers. However, females often participated in parental care and in some cases assumed the typical male role in the absence of the male. In the presence of her mate, females generally performed different care-giving functions than males. Females attended broods at a distance and chased other fishes more frequently than males. Males remained directly over the brood guarding. A series of mated pairs in each of three reproductive conditions were captured and examined. Different pairs were compared between reproductive conditions for body weight, body condition, gonadal-somatic index, and a gut-contents index. The inital costs of reproduction, as measured by weight loss, condition change, and gonadal-somatic index change, were more severe in females than males. During breeding and subsequent care-giving, males did little or no feeding whereas females increased their feeding during the same time period. However, males appeared to sustain only minor weight and condition losses due to care-giving. I suggest that males were the principal care-givers because the net benefits of remaining at the nest were greater than the net benefits of leaving. Males had little opportunity to mate with more than one female each season, and offspring had little chance of survival in the absence of a care-giving adult. Considerable variation in female behavior occurred which suggests that the net benefits of care-giving were nearly balanced with the net benefits of leaving the brood. The relative importance of feeding versus care-giving by females may vary with slight differences between females and the behavior of their mates as care-givers.Present address: Department of Zoology, Ohio State University, 1735 Neil Avenue, Columbus, Ohio 43210, USA     

Lifetime reproductive success in the spotted sandpiper (Actitis macularia) : sex differences and variance components

Summary Lifetime reproductive success (LRS) of male (N=103) and female (N= 66) spotted sandpipers (Actitis macularia) was studied for 13 years of a 17-year study at Little Pelican Island, Leech Lake, Minnesota. There was no sex difference in longevity, but females had significantly more mates, eggs, chicks, fledged young, and young returning in subsequent years than did males. Variance in LRS was partitioned into five life-history components: longevity (L), mates per year (M), eggs per mate (E), proportion eggs hatched (H), and proportion of chicks fledged (F). For both sexes, F accounted for the greatest proportion of variance in LRS (males, 43%; females, 47%), followed by L (males, 26%; females, 43%) and H (males, 21%; females, 28%). Positive covariance between H and F was consistent with predator-caused clutch and brood loss. Contrary to our expectations, males had a higher coefficient of variation in reproductive success than did females. This was because males were relatively more likely than females to produce no young.Offprint requests to: L.W. Oring at the current address     

Male choice and competition in Tetraopes tetraophthalmus: effects of local sex ratio variation

Summary Male milkweed beetles (Tetraopes tetraophthalmus) are shown to exhibit choice between potential mates. Males, however, also exhibit direct competition for access to potential mates. These differences in male behavior are dependent on the local sex ratio, with males becoming increasingly choosy when the sex ratio is female-biased, and more competitive when the sex ratio is malebiased. Females show neither choice nor competition. In both the laboratory and in the field, body size is important in determining patterns of competition and choice. Larger males win most aggressive encounters, and males generally prefer large females as mates. The combination in a single sex, of competition for mates and mate choice is not predicted by classical sexual selection theory. Male choice and competition may have evolved in T. tetraophthalmus due to the combination of (1) the mating system (2) the pattern of variation in female fecundity, and (3) the spatially and temporally variable operational sex ratios. This explanation is not dependent on high heritability of body size.     

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.