Mating portfolios: bet-hedging, sexual selection and female multiple mating

García‐González, Francisco; Yasui, Yukio; Evans, Jonathan P.

doi:10.1098/rspb.2014.1525

Cited by 44 publications

(65 citation statements)

References 51 publications

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“…Exact p-values would probably be larger, due to additional variance in the population that is not captured by the sample. Table 1 shows that most of the comparisons made by GarciaGonzalez et al [1] yielded results consistent with the null hypothesis (a ¼ 0.05) after reanalysis, suggesting that fitness did not differ significantly between polyandry and monandry treatments. Nevertheless, the estimated 95% CIs often included large differences, suggesting that this dataset does not rule out the existence of a substantial benefit from bet-hedging via polyandry.…”

Section: Null Hypothesis Significance Testingsupporting

confidence: 70%

“…Garcia-Gonzalez et al [1] compared the fitness of females under experimentally imposed monandry and polyandry. The eggs of 12 females were divided into three batches, representing three 'generations'.…”

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confidence: 99%

“…Bet-hedging via polyandry: a comment on 'Mating portfolios: bet-hedging, sexual selection and female multiple mating' Jonathan M. Henshaw and Luke Holman Division of Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, Australia Garcia-Gonzalez et al [1] conducted an original and elegant experiment examining whether fertilization of a female's eggs by multiple males ( polyandry) can provide fitness benefits via 'bet-hedging' (i.e. due to decreased variance in offspring fitness).…”

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confidence: 99%

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Bet-hedging via polyandry: a comment on ‘Mating portfolios: bet-hedging, sexual selection and female multiple mating’

Henshaw

Holman

2015

Proc. R. Soc. B.

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Garcia-Gonzalez et al.[1] conducted an original and elegant experiment examining whether fertilization of a female's eggs by multiple males ( polyandry) can provide fitness benefits via 'bet-hedging' (i.e. due to decreased variance in offspring fitness). The authors measured these benefits in both stable and variable environments, and also quantified the joint fitness consequences of bet-hedging and sperm competition. We believe that the study's experimental design is sound, but that its statistical analysis was incorrect. Here, we reanalyse the raw data and find that all but one of the study's results is consistent with the null hypothesis that polyandry does not provide benefits via bet-hedging, contrary to the original conclusions.Garcia-Gonzalez et al.[1] compared the fitness of females under experimentally imposed monandry and polyandry. The eggs of 12 females were divided into three batches, representing three 'generations'. For each female and generation, half of the eggs were fertilized using the sperm of a single male (monandry) and the other half with sperm from three males (polyandry). The authors measured fertilization rates and offspring viability (the latter in two different environments, termed A and B) for each of the 12 females and three generations.From the viability and fertilization data, the authors calculated the betweengeneration geometric means of each fitness measure (W BG ) under polyandry and monandry, and calculated the difference in W BG between treatments as(1:1)A positive value of D Geo implies that polyandry improves geometric mean fitness. To account for variation in D Geo due to the arbitrary ordering of generations, the authors repeated this calculation 10 4 times while randomly varying the order of generations for each female, and generated 95% central ranges for D Geo , which they took as approximate confidence intervals. Similar randomization procedures were used to simulate various regimes of stable and fluctuating environmental conditions. This method of generating confidence intervals is problematic. It accounts for one source of variation in the sample (i.e. the ordering of generations) but neglects the variance that results from sampling a finite number of males, females and offspring from the population. This causes the analysis to substantially underestimate the size of the confidence intervals around D Geo , and thereby to produce false positives.Moreover, we believe that the geometric mean is not the most appropriate fitness measure for Garcia-Gonzalez et al.'s analysis. In cases where (i) the absolute fitness of each strategy comes from the same probability distribution in all generations and (ii) fitness is uncorrelated among individuals of the same genotype (here, monandrous and polyandrous females), it is more appropriate to apply Gillespie's measure [2-4]here m i and s 2 i are the population mean and variance in reproductive success of each strategy within a generation, and N is the population size. The assumptions behind Gillespie's measure are met for those t...

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Section: Null Hypothesis Significance Testingsupporting

confidence: 70%

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confidence: 99%

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Bet-hedging via polyandry: a comment on ‘Mating portfolios: bet-hedging, sexual selection and female multiple mating’

Henshaw

Holman

2015

Proc. R. Soc. B.

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confidence: 87%

“…We want to clarify that this comment about pseudoreplication applies to HH's analysis, not to our experiment or analyses, as the above statement may seem to imply to the reader. Females in our experiment represent distinct genotypes that are assayed across three generations each (this is the purpose of the design); our analysis takes this fact into account and estimates intergenerational fitness accordingly [2]. As for males, they are not used across generations or across blocks (females).…”

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Risk-spreading by mating multiply is plausible and requires empirical attention

2015

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We appreciate Henshaw & Holman's [1] (henceforth HH) comment regarding our original article [2]. We understand the points made by HH, but we have reservations about their applicability to our data, as explained below. Before addressing the specific details in HH's commentary, however, it is important to note that the substance of their article deals with technical aspects of our statistical analysis, not the underlying theoretical framework or the empirical design employed in our study. Indeed, we are happy to see that HH acknowledge that our work offers a valid proof-of-principle approach for studying the role that bet-hedging plays in determining the benefits of multiple mating in isolation from other factors, namely sexually selected mechanisms. Indeed, that was the main motivation of our study, rather than to specifically document the benefits of bet-hedging and sexual selection in the subject species.To briefly recap, our study revisited the concept of bet-hedging in the context of explaining female multiple mating, identified common misunderstandings surrounding its interpretation and offered a novel experimental approach to test for its existence. Our study system, the sea urchin Heliocidaris erythrogramma armigera, offers remarkable levels of experimental control via in vitro fertilizations, thus enabling us to analyse temporal (geometric mean) fitness among females assigned simultaneously to a polyandrous and monandrous mating strategy. In this way, we controlled for the effects of female genotype and maternal effects on fitness outcomes, while separating 'pure' bet-hedging effects from sexually selected paternity-biasing mechanisms by manipulating the fertilization conditions (presence or absence of competition among the gametes of different males). The underlying question addressed in our paper was to determine whether the intergenerational fitness of females is higher when they follow a strategy that increases mate sampling (i.e. polyandry) compared with a non-bet hedger strategy (monandry). By simulating reproductive bouts across generations, we uncovered the potential for bet-hedging, in addition to paternity-biasing mechanisms (e.g. sexual selection), to provide increases in fitness for multiply mated females.HH's first comment suggests that technically, Gillespie's measure may provide a more appropriate fitness measures for our data. We appreciate the suggestion here, but note that Gillespie's measure hardly deviates from our use of geometric mean fitness, which can be understood as a valid proxy of intergenerational fitness (e.g. compare, for each trait, the data in the first and third rows in the first column of HH's table 1). Second, HH acknowledge that the analysis of alternating environments of the form ABA and BAB requires complex analysis. However, in the event, HH do not carry out such analysis. Instead, they apply bootstrapping to estimate confidence intervals (CIs) on mean effect sizes using our measure of evolutionary fitness (geometric mean) and Gillespie's measure. If the main objec...

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Polyandry and Mating System Evolution

Boulton

2020

Encyclopedia of Life Sciences

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Our understanding of animal mating systems has been considerably enhanced in recent years by the development of molecular methods to reliably assay female multiple mating (polyandry). These techniques have demonstrated that polyandry is widespread across animal groups, even in species thought to be strictly monogamous and pair‐bonded. The research that has arisen from this paradigm shift has shown that females can gain substantial material benefits from mating with multiple males, in terms of increased fecundity, infanticide avoidance and sperm replenishment. Polyandry can also provide indirect or genetic benefits to females, increasing the likelihood that they will mate with at least one compatible or high‐quality male. By mating multiply females can also increase the genetic diversity of their offspring, which may be advantageous in changeable environments. Importantly polyandry has demonstrated that mating systems extend beyond copulation and sexual selection occurs not just over mates but also over their gametes. Key Concepts Recent developments in molecular ecology have allowed researchers to rapidly and easily test whether multiple fathers sire female offspring. Multiple mating by females (polyandry) is now known to be widespread across taxa. While mating can be costly, polyandry has been shown to provide substantial benefits to females. Direct, or material benefits of polyandry increase female offspring production, for instance by providing females with additional resources in nuptial gifts or seminal fluids. Indirect, or genetic benefits of polyandry arise when multiple mating increases the chances that a female mates with at least one compatible or high‐quality male. Polyandry can also increase offspring genetic diversity, and this can be beneficial in unstable or harsh environments, increasing the chances that at least some offspring will survive. Polyandry means that sexual selection continues after mating, males compete not only for mates but also their gametes (post‐copulatory sexual selection). Post‐copulatory sexual selection can render certain male traits beneficial, which can alter the costs and benefits of polyandry for females and change the optimal female mating rate. As a result of the realisation that polyandry is widespread, mating systems research now integrates formerly unappreciated concepts such as sperm competition, cryptic female choice and co‐evolutionary feedbacks between male and female mating strategies.

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Mating portfolios: bet-hedging, sexual selection and female multiple mating

Cited by 44 publications

References 51 publications

Bet-hedging via polyandry: a comment on ‘Mating portfolios: bet-hedging, sexual selection and female multiple mating’

Bet-hedging via polyandry: a comment on ‘Mating portfolios: bet-hedging, sexual selection and female multiple mating’

Risk-spreading by mating multiply is plausible and requires empirical attention

Polyandry and Mating System Evolution

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