The evolutionary dynamics of adaptive virginity, sex-allocation, and altruistic helping in haplodiploid animals

In females of haplodiploid animals, female production requires fertilization, whereas male production does not. Therefore, haplodiploid species can display extraordinary sex ratios. Constrained sex allocation occurs when a female cannot produce daughters. This can be due to virginity but may also occur after mating due to insemination failure, selfish genetic elements or physiological constraints. Here, we investigated the mechanism underlying constrained sex allocation in Pezothrips kellyanus. In this species some mated females produce highly female‐biased broods, yet, for unknown reasons, others produce extremely male‐biased broods. Using crossing experiments controlled for maternally inherited endosymbionts we confirmed that constrained females were successfully inseminated. Furthermore, male‐biased offspring production was not paternally inherited, ruling out paternal sex ratio elements previously identified as sex ratio distorters in some parasitoid wasps. Next, we excluded mating time and paternal fitness effects (male size) on sex allocation. However, we found that constrained sex allocation only occurred in small females producing smaller eggs than large females producing larger eggs and female‐biased broods. Consequently, the bimodal sex allocation pattern correlates with maternal condition, and may have arisen (adaptively or non‐adaptively) in association with an egg size‐mediated fertilization mechanism recently detected in some haplodiploids, with egg size positively affecting fertilization success.

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“…2008; Rautiala et al. 2018), but less extensively so in other haplodiploid taxa (e.g., Higgins and Myers 1992; Kranz et al. 2000).…”

Section: Figurementioning

confidence: 99%

Constrained sex allocation after mating in a haplodiploid thrips species depends on maternal condition

et al. 2021

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“…Ours is an ‘open model’ (sensu (21)) where some parameters, notably the probability that a female is unmated and the sex ratio produced by the mated ones, are evaluated at every possible combination, rather than restricting the view to those combinations that are more likely to be found in nature. In reality, if many sons will be produced by virgin mothers, there will be selection on mated mothers to specialize in the production of females, more so than they would in the absence of virgin reproducers (22). Effectively, this means that the most likely areas of our surface plots found in nature are those that do not feature unrealistically high proportions of males.…”

Section: Discussionmentioning

confidence: 99%

Sex ratio and sexual conflict in a collective action problem

Lindstedt

Gerber

Kokko

2020

Preprint

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The maintenance of cooperation is difficult whenever collective action problems are vulnerable to freeriding (reaping the benefits without contributing to the maintenance of the good). We identify a novel factor that can make a system tolerate an extent of freeriding. If a population consists of discrete types with demographically distinct roles, such that the success of one type does not imply it can spread to replace other types in the population, then collective goods may persist in the presence of free-riders because they are necessarily kept in a minority role. Biased sex ratios (e.g. in haplodiploids) create conditions where individuals of one sex are a minority. We show that this can make the less common sex contribute less to a public good in a setting where the relevant life-history stage — larval group defence against predators — does not feature any current breeding opportunities that might lead to confounding reasons behind sex-specific behaviour. We test our model with haplodiploid pine sawfly larvae, showing that female larvae are the main contributors to building the antipredator defence against predators.Significance statementIndividuals in groups can cooperate to achieve something together, but with an evolutionary difficulty: if benefits of cooperation are shared equally among all, freeriders get the same benefit as others while paying less for it. We propose a novel reason why freeriding does not automatically spread until the collectively beneficial outcome is destroyed: sometimes groups consist of individuals of distinct categories, limiting freerider spread. If, for example, there are always fewer males than females, then even if every male becomes a freerider, the whole group still survives simply because not everyone can be male. Pine sawfly larvae defend against predators by regurgitating sticky fluids, but females contribute more to this common defence, and we show this example fits our model.

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“…(), but may nevertheless be play a role when combined with a bivoltine life cycle (Quiñones and Pen ) or adaptive virginity (Rautiala et al. ; this study also used the benefit threshold approach and a stable population size). Whether the insights of the current analysis would impact these other mechanisms is yet an open question.…”

Section: Discussionmentioning

confidence: 99%

Extended haplodiploidy hypothesis

2019

Self Cite

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Evolution of altruistic behavior was a hurdle for the logic of Darwinian evolution. Soon after Hamilton formalized the concept of inclusive fitness, which explains how altruism can evolve, he suggested that the high sororal relatedness brought by haplodiploidy could be why Hymenopterans have a high prevalence in eusocial species, and why helpers in Hymenoptera are always female. Later it was noted that in order to capitalize on the high sororal relatedness, helpers would need to direct help toward sisters, and this would bias the population sex ratio. Under a 1:3 males:females sex ratio, the inclusive fitness valuation a female places on her sister, brother, and an own offspring are equal—apparently removing the benefit of helping over independent reproduction. Based on this argumentation, haplodiploidy hypothesis has been considered a red herring. However, here we show that when population sex ratio, cost of altruism, and population growth rate are considered together, haplodiploidy does promote female helping even with female‐biased sex ratio, due the lowered cost of altruism in such populations. Our analysis highlights the need to re‐evaluate the role of haplodiploidy in the evolution of helping, and the importance of fully exploring the model assumptions when comparing interactions of population sex ratios and social behaviors.

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The evolutionary dynamics of adaptive virginity, sex-allocation, and altruistic helping in haplodiploid animals

Cited by 12 publications

References 47 publications

Constrained sex allocation after mating in a haplodiploid thrips species depends on maternal condition

Constrained sex allocation after mating in a haplodiploid thrips species depends on maternal condition

Sex ratio and sexual conflict in a collective action problem

Extended haplodiploidy hypothesis

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