Haplodiploidy and the Evolution of Eusociality: Worker Revolution

Alpedrinha, João; Gardner, Andy; West, Stuart A.

doi:10.1086/677283

Cited by 13 publications

(11 citation statements)

References 52 publications

(72 reference statements)

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“…The theoretical grounds are that when both sexes are properly accounted for in the inclusive fitness calculations, haplodiploidy requires female-biased sex ratios to favour eusociality8. However, recent models suggest that the conditions (polyandry, see above) which favour such biased sex ratios are unlikely to have been present in the early evolution of eusociality254546. Here we have shown that, depending on the type of bivoltine life cycle, haplodiploidy can both inhibit and promote the evolution of reproductive altruism.…”

Section: Discussionmentioning

confidence: 71%

“…The favourable effects that lifetime monogamy has on the evolution of reproductive altruism and cooperative breeding have both considerable theoretical20254546 and empirical support. Strict parental monogamy has now been well documented as the ancestral state across lineages of the social Hymenoptera and termites with permanent worker castes4748, but the mechanisms are very different.…”

Section: Discussionmentioning

confidence: 99%

“…Hamilton’s idea that haplodiploidy favours the evolution of reproductive altruism has been challenged on both empirical and theoretical grounds78102546. The empirical grounds are that reproductive altruism occurs also in several diploid species7.…”

Section: Discussionmentioning

confidence: 99%

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A unified model of Hymenopteran preadaptations that trigger the evolutionary transition to eusociality

Quiñones

Pen

2017

Nat Commun

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Explaining the origin of eusociality, with strict division of labour between workers and reproductives, remains one of evolutionary biology’s greatest challenges. Specific combinations of genetic, behavioural and demographic traits in Hymenoptera are thought to explain their relatively high frequency of eusociality, but quantitative models integrating such preadaptations are lacking. Here we use mathematical models to show that the joint evolution of helping behaviour and maternal sex ratio adjustment can synergistically trigger both a behavioural change from solitary to eusocial breeding, and a demographic change from a life cycle with two reproductive broods to a life cycle in which an unmated cohort of female workers precedes a final generation of dispersing reproductives. Specific suits of preadaptations are particularly favourable to the evolution of eusociality: lifetime monogamy, bivoltinism with male generation overlap, hibernation of mated females and haplodiploidy with maternal sex ratio adjustment. The joint effects of these preadaptations may explain the abundance of eusociality in the Hymenoptera and its virtual absence in other haplodiploid lineages.

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Section: Discussionmentioning

confidence: 71%

Section: Discussionmentioning

confidence: 99%

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A unified model of Hymenopteran preadaptations that trigger the evolutionary transition to eusociality

Quiñones

Pen

2017

Nat Commun

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“…The early stages in the evolution of life required cooperation between simple replicators, which may also have been favoured due to population structure keeping relatives together 131,132 . In contrast, while the possible role of haplodiploid genetics has attracted much attention, both theory and empirical data have led to many concluding that it was a red herring [133][134][135][136][137][138][139] .…”

Section: Indirect Benefits Play the Major Role In Explaining Cooperation Within Speciesmentioning

confidence: 99%

Ten recent insights for our understanding of cooperation

et al. 2021

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Since Hamilton published his seminal papers in 1964, our understanding of the importance of cooperation for life on earth has evolved beyond recognition. Early research was focused on altruism in the social insects, where the problem of cooperation was easy to see. In more recent years, research into cooperation has expanded across the entire tree of life, and has been revolutionised by advances in genetic, microbiological, and analytical techniques. We highlight ten insights that have arisen from these advances, which have illuminated generalisations across different taxa, making the world simpler to explain. Furthermore, progress in these areas has opened up numerous new problems to solve, suggesting exciting directions for future research. Relatedness: from anecdotes to broad generalisationsInclusive fitness theory shows how cooperation can be favoured by kin selection if it is directed towards relatives, who carry the gene for cooperation (relatives) 2 (Box 1). But how widespread is the importance of kin selection? And if it is important, how do we explain variation between individuals in the level of cooperation, or explain why cooperation is favoured in some species and not others?Recent research has shown that the relatedness (R) between interacting individuals has a clear and consistent influence on the evolution of cooperation, with both theory and data suggesting that the same factors play analogous roles at all levels of biology, from simple replicators and viruses, to complex animal groups (see below; Supplementary Tables 1 & 2). This role of relatedness has been demonstrated with a combination of methodologies, including observational, experimental, experimental evolution, across-species comparisons, and genomic.1a. Group formation. Consistent with kin selection favouring cooperation, there is considerable evidence that population structure and how groups form is a major determinant of whether cooperation is favoured 2 (Fig. 2).(i) Individuals are more cooperative in species where social groups form by staying together, compared with species where social groups form by aggregation, across a range of taxa, including bacteria, fungi, slime moulds, insects, and birds [19][20][21][22][23] .(ii) Individuals are more cooperative in species where females mate monogamously or with few males, in birds, mammals, insects and shrimps 13,19,21,[24][25][26] .(iii) When population structure is manipulated experimentally, in a range of microorganisms, including bacteria, fungi and viruses, the conditions which lead to high relatedness favour greater cooperation 15,[27][28][29][30][31][32] .(iv) The role of group formation has also been supported by sequence data. If a trait is favoured by kin selection, then lower relatedness will lead to weaker selection for that trait, and so the removal of deleterious mutations will be slower and less likely [33][34][35][36] . Consistent with kin selection playing an important role: (a) ant and bee species with either multiple mating or multiple queens, and hence reduced relatedn...

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“…Hamilton, 1964;Lehmann et al, 2008;Boomsma, 2009), bivoltinism and asymetrical sex-ratio (e.g. Trivers and Hare, 1976;Seger, 1983;Alpedrinha et al, 2014;González-Forero, 2015;Quiñones and Pen, 2017), coercion (i.e. policing, Wenseleers et al, 2004;Dobata, 2012), queen longevity and competition between queens (e.g.…”

Section: Introductionmentioning

confidence: 99%

Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

Weyna

Romiguier

Mullon

2021

Preprint

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The success of a eusocial colony depends on two main castes: queens that reproduce and sterile workers that help them. This division of labour is vulnerable to selfish genetic elements that enforce the development of their carriers into queens. Several factors, e.g. intra-colonial relatedness, can influence the spread of such selfish elements. Here we investigate a common yet understudied ecological setting: where hybrid larvae can develop into workers. Using mathematical modelling, we show that the coevolution of hybridization with caste determination readily triggers an evolutionary arms race between larvae that increasingly develop into queens, and queens that increasingly hybridize to produce workers. Even where hybridization reduces fitness, this race can lead to the loss of developmental plasticity and genetically hard-wired caste determination. Overall, our results help understand the repeated evolution towards complex reproductive systems (e.g. social hybridogenesis) and the special forms of parasitism (e.g. inquilinism) observed in many eusocial insects.

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Haplodiploidy and the Evolution of Eusociality: Worker Revolution

Cited by 13 publications

References 52 publications

A unified model of Hymenopteran preadaptations that trigger the evolutionary transition to eusociality

A unified model of Hymenopteran preadaptations that trigger the evolutionary transition to eusociality

Ten recent insights for our understanding of cooperation

Hybridization enables the fixation of selfish queen genotypes in eusocial colonies

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