Maydianne C. B. Andrade

Sexual Selection for Male Sacrifice in the Australian Redback Spider

During copulation, male redback spiders (Latrodectus hasselti: Theridiidae) position themselves above the females jaws. This apparent male complicity in sexual cannibalism is favored by sexual selection because cannibalized spiders receive two paternity advantages. First, cannibalized males copulated longer and fertilized more eggs than those that survived copulation. Second, females were more likely to reject subsequent suitors after consuming their first mate. These results represent empirical evidence for male copulatory suicide as an adaptive behavior.

FEMALE CHOICE FOR AN INDICATOR OF MALE SIZE IN THE SONG OF THE BLACK-HORNED TREE CRICKET, OECANTHUS NIGRICORNIS (ORTHOPTERA: GRYLLIDAE: OECANTHINAE)

The calling song of male crickets, including Oecanthus nigricornis (Walker), attracts females for mating and provides a model system of sexual communication. We give the first conclusive identification of a feature of cricket song that is both attractive to females and indicates a phenotypic feature (body size) that determines male mating success and female reproductive benefits. We do this by first testing for correlations between song characteristics and aspects of male phenotype that are hypothesized to indicate male quality. We show that song is a reliable indicator of male size and male age, and that large male size is associated with increased female fecundity. We then use playbacks of synthetic songs that mimic natural variation in song parameters to study song preferences and we compare preferences under different presentation regimes to determine whether choices are based on relative song quality or some fixed criterion. Females show a preference for the lower frequency songs produced by large males, but only during simultaneous playbacks. Thus female choice is based on the relative quality of calls that can be sampled simultaneously. These results provide strong support for the hypothesis that females use variation in calling song to assess male mate quality.

Spatial and temporal demographic variation drives within-season fluctuations in sexual selection.

Abstract Our understanding of selection in nature stems mainly from whole-season and cross-sectional estimates of selection gradients. These estimates suggest that selection is relatively constant within, but fluctuates between seasons. However, the strength of selection depends on demographics, and because demographics can vary within seasons, there is a gap in our understanding regarding the extent to which seasonal fluctuations in demographics may cause variation in selection. Here we use two populations of the golden orb-web spider (Nephila plumipes) that differ in density to examine how demographics change within a season and whether there are correlated shifts in selection. We demonstrate that there is within-season variation in sex ratio and density at multiple spatial and temporal scales. This variation led to changes in the competitive challenges that males encountered at different times of the season and was correlated with significant variation in selection gradients on male size and weight between sampling periods. We highlight the importance of understanding the biology of the organism under study to correctly determine the relevant scale in which to examine selection. We also argue that studies may underestimate the true variation in selection by averaging values, leading to misinterpretation of the effect of selection on phenotypic evolution.

Value of male remating and functional sterility in redback spiders

In the Australian redback spider, Latrodectus hasselti, males typically use their paired copulatory organs (palps) to copulate twice with a single female then sacrifice themselves to their cannibalistic mates in a strategy that increases their paternity in that one mating, but leads to death. This type of terminal investment in one mating is predicted only if the expected value of future matings is low for males relative to the value of repeated mating with the same female. In this laboratory study, we quantified the reproductive value of mating more than once with the same female (repeated mating) and mating with more than one female (multiple mating) for male redback spiders. We tested two natural selection hypotheses for repeated mating, sperm limitation and reproductive insurance, but found no support for either hypothesis. We show that, in the absence of sperm competition or cannibalism, male lifetime reproductive output is the same whether a male copulates once, twice, or several times with a given female. Repeated mating does not increase the probability of successful fertilization, nor does it increase the number of offspring produced in successful matings. Although male repeated mating is not favoured because of increased fertility of mates, other studies suggest it may be important in sperm competition. Here we show that the relative reproductive value of the first two copulations is very high for redback males because they are functionally sterile after each palp has been used once; nonvirgin males are unable to father offspring. Functional sterility and repeated mating by male redbacks may be favoured by the same factors that lead to male sacrifice behaviour: ecological constraints on multiple mating combined with competitive benefits of maximal investment in the first mating. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.

Multiple sperm storage organs facilitate female control of paternity.

It has been proposed that multiple sperm storage organs (spermathecae) could allow polyandrous females to control paternity. There is little conclusive evidence for this since insemination of individual spermathecae is generally not experimentally manipulable. Here, we examined sperm use patterns in the Australian redback spider (Latrodectus hasselti), which has paired, independent spermathecae. We assessed paternity when two rivals were forced to inseminate a single storage organ or opposite storage organs. When males inseminated a single spermatheca, mean paternity of the females first mate was 79.8% (median 89.4%), and 38% of first mates achieved 100% paternity. In contrast, when males inseminated opposite organs, the mean paternity of the first mate was 49.3% (median 49.9%), only 10% of males achieved complete precedence, and paternity was normally distributed, suggesting sperm mixing. Males responded to this difference by avoiding previously inseminated female reproductive tracts. Complete sperm precedence can only be achieved if females permit males to copulate with both reproductive tracts. Females often cannibalize smaller males during their first copulation, thus limiting their paternity to 50%. These data show that multiple sperm storage organs can increase female control of paternity.

Terminal Investment Strategies and Male Mate choice: Extreme Tests of Bateman'

Abstract Batemans principle predicts the intensity of sexual selection depends on rates of increase of fecundity with mating success for each sex (Bateman slopes). The sex with the steeper increase (usually males) is under more intense sexual selection and is expected to compete for access to the sex under less intense sexual selection (usually females). Under Bateman and modern refinements of his ideas, differences in parental investment are key to defining Bateman slopes and thus sex roles. Other theories predict sex differences in mating investment, or any expenditures that reduce male potential reproductive rate, can also control sex roles. We focus on sexual behaviour in systems where males have low paternal investment but frequently mate only once in their lifetimes, after which they are often killed by the female. Mating effort (=terminal investment) is high for these males, and many forms of investment theory might predict sex role reversal. We find no qualitative evidence for sex role reversal in a sample of spiders that show this extreme male investment pattern. We also present new data for terminally-investing redback spiders (Latrodectus hasselti). Bateman slopes are relatively steep for male redbacks, and, as predicted by Bateman, there is little evidence for role reversal. Instead, males are competitive and show limited choosiness despite wide variation in female reproductive value. This study supports the proposal that high male mating investment coupled with low parental investment may predispose males to choosiness but will not lead to role reversal. We support the utility of using Bateman slopes to predict sex roles, even in systems with extreme male mating investment.

Males assess chemical signals to discriminate just-mated females from virgins in redback spiders

In species where virgin females have higher reproductive value to males than nonvirgin females, selection will favour males that can discriminate female reproductive status. Similarly, while virgin females may actively seek to attract males, nonvirgin females may seek crypticity after mating if copulation is costly. Here we show that Australian redback spider males, Latrodectus hasselti, discriminate female maturity and mating status based exclusively on web-borne chemicals. Male activity on extracts from webs of virgin females significantly exceeded activity on extracts of webs of juveniles, nonvirgin females and solvent controls. While this level of discernment of female reproductive status has been found in other spiders, here we show that discrimination of web-bound chemicals produced by virgin females disappears rapidly after these females mate. Extracts of webs built by females immediately after copulation elicited no more interest from males than did solvent controls. Redback males dismantle much of their mates web during courtship, and these results suggest that the web rebuilt by females after mating would not trigger male courtship. We speculate that this rapid shift would significantly reduce the opportunity for polyandry in nature.

Male development tracks rapidly shifting sexual versus natural selection pressures

Document S1. Supplemental Experimental ProceduresxDownload (.1 MB ) Document S1. Supplemental Experimental Procedures

A change in competitive context reverses sexual selection on male size

In studies of sexual selection, larger size is often argued to increase male fitness, and relatively smaller males are explained by genetic and/or environmental variation. We demonstrate that a size–development life‐history trade‐off could underlie the maintenance of a broad, unimodal distribution of size in male redback spiders (Latrodectus hasselti). Larger males are superior in direct competition, but redback males mature rapidly at small size in the presence of females. In field enclosures, we simulated two competitive contexts favouring development of divergent male sizes. Relatively smaller males lost when competing directly, but had 10 times higher fitness than relatively larger males when given the temporal advantage of rapid development. Linear selection gradients confirmed the reversal of selection on size, showing that it is critical to consider life‐history decisions underlying the development of traits related to fitness.

Evidence for developmental plasticity in response to demographic variation in nature.

Adaptive developmental plasticity has been demonstrated across a number of taxa in response to variables such as photoperiod, resource abundance, and predator presence. Demographics also vary temporally and spatially within populations, but few studies have examined the possibility that developmental plasticity in response to changes in these variables can alter phenotypic distributions. Plastic responses to variable population density and sex ratio may play an important role in explaining phenotypic variation in nature. In this study, we examine two species of spiders (Nephila plumipes and Argiope keyserlingi) to examine whether there is evidence that males alter their development in response to demographics in natural populations. We studied spiders in which developing males can use pheromones as a cue of the density of conspecific males and females. We used published information about the mating systems and life history of each species to make predictions about expected patterns of plasticity in development time and correlated changes in adult body size in response to demographic variation. Within each species, male size and mass were positively correlated with the density of males but negatively correlated with the density of females, and as predicted, this was true only when calculated at spatial scales relevant to selection in each species. In contrast, seasonal variation in photoperiod could not explain measured variance in male size. Our results support the idea that developmental plasticity in response to demographics has a significant effect on phenotypic distributions in natural populations. Our results suggest that a proportion of variation in male phenotypes could be explained as a plasticity-mediated evolutionary response to variation in population demographics rather than as a physiological response to resource abundance and/or photoperiod.