An Organismal Perspective on the Evolution of Insect Societies

Helanterä, Heikki

doi:10.3389/fevo.2016.00006

Cited by 28 publications

(37 citation statements)

References 108 publications

(158 reference statements)

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“…However, these reviews left the connection with superorganismality open‐ended, and Boomsma (, p. 2) erroneously credited Batra (1966 a ) for defining eusociality as being based on morphological caste differentiation. After our present historical analysis of eusociality and superorganismality, the conclusion must be that hypersociality sensu Batra () and obligate eusociality sensu Crespi & Yanega () and Boomsma (, , ) are functionally identical to superorganismality sensu Wheeler (), defined by permanent membership of each colony member to a single morphologically distinct adult caste that is fixed for life during early individual development (Wheeler, ; Helanterä, ) (Fig. ; Table , qE4, qE17, qE21, qE22, qS3, qS6 and qS7).…”

Section: Historymentioning

confidence: 97%

Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation

2017

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More than a century ago, William Morton Wheeler proposed that social insect colonies can be regarded as superorganisms when they have morphologically differentiated reproductive and nursing castes that are analogous to the metazoan germ-line and soma. Following the rise of sociobiology in the 1970s, Wheeler's insights were largely neglected, and we were left with multiple new superorganism concepts that are mutually inconsistent and uninformative on how superorganismality originated. These difficulties can be traced to the broadened sociobiological concept of eusociality, which denies that physical queen-worker caste differentiation is a universal hallmark of superorganismal colonies. Unlike early evolutionary naturalists and geneticists such as Weismann, Huxley, Fisher and Haldane, who set out to explain the acquisition of an unmated worker caste, the goal of sociobiology was to understand the evolution of eusociality, a broad-brush convenience category that covers most forms of cooperative breeding. By lumping a diverse spectrum of social systems into a single category, and drawing attention away from the evolution of distinct quantifiable traits, the sociobiological tradition has impeded straightforward connections between inclusive fitness theory and the major evolutionary transitions paradigm for understanding irreversible shifts to higher organizational complexity. We evaluate the history by which these inconsistencies accumulated, develop a common-cause approach for understanding the origins of all major transitions in eukaryote hierarchical complexity, and use Hamilton's rule to argue that they are directly comparable. We show that only Wheeler's original definition of superorganismality can be unambiguously linked to irreversible evolutionary transitions from context-dependent reproductive altruism to unconditional differentiation of permanently unmated castes in the ants, corbiculate bees, vespine wasps and higher termites. We argue that strictly monogamous parents were a necessary, albeit not sufficient condition for all transitions to superorganismality, analogous to single-zygote bottlenecking being a necessary but not sufficient condition for the convergent origins of complex soma across multicellular eukaryotes. We infer that conflict reduction was not a necessary condition for the origin of any of these major transitions, and conclude that controversies over the status of inclusive fitness theory primarily emanate from the arbitrarily defined sociobiological concepts of superorganismality and eusociality, not from the theory itself.

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Section: Historymentioning

confidence: 97%

Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation

2017

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“…We showed that when dynamic properties of resource allocation are considered, sex allocation conflict can substantially affect colony ontogeny, and thus overall patterns of growth and productivity. Helanterä (2016) has argued that life-history trade-offs may be easier traits to conceptualize as organismal traits (i.e. traits evolving like group-selected adaptations), as opposed to traits more heavily contingent on conflicts among genes in different individuals, such as traits involving sex allocation and dispersal behaviour.…”

Section: Resultsmentioning

confidence: 99%

Sex allocation conflict and sexual selection throughout the lifespan of eusocial colonies

Avila

Fromhage

Lehmann

2018

Preprint

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Models of sex allocation conflict are central to evolutionary biology but have mostly assumed static decisions, where resource allocation strategies are constant over colony lifespan. Here, we develop a model to study how the evolution of dynamic resource allocation strategies is affected by the queen-worker conflict in annual eusocial insects. We demonstrate that the time of dispersal of sexuals affects the sex allocation ratio through sexual selection on males. Furthermore, our model provides three predictions that depart from established results of classic static allocation models. First, we find that the queen wins the sex allocation conflict, while the workers determine the maximum colony size and colony productivity. Second, malebiased sex allocation and protandry evolve if sexuals disperse directly after eclosion. Third, when workers are more related to new queens, then the proportional investment into queens is expected to be lower, which results from the interacting effect of sexual selection (selecting for protandry) and sex allocation conflict (selecting for earlier switch to producing sexuals). Overall, we find that colony ontogeny crucially affects the outcome of sex-allocation conflict because of the evolution of distinct colony growth phases, which decouples how queens and workers affect allocation decisions and can result in asymmetric control.

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“…Evolution of caste‐biased gene expression in social insects has interesting similarities to evolution of tissue‐specific gene expression. Indeed, if an insect society is seen as a superorganism, queens and workers are analogous to reproductive and somatic tissues, respectively (Helanterä ). As with social insect castes, it seems that genes with a tissue‐specific expression profile are prone to fast evolution due to low pleiotropic constraint (Duret et al.…”

Section: Discussionmentioning

confidence: 99%

“…Evolution of caste-biased gene expression in social insects has interesting similarities to evolution of tissue-specific gene expression. Indeed, if an insect society is seen as a superorganism, queens and workers are analogous to reproductive and somatic tissues, respectively (Helanterä 2016). As with social insect castes, it seems that genes with a tissue-specific expression profile are prone to fast evolution due to low pleiotropic constraint (Duret et al 1999), but it remains an open question whether genes with little constraint have been co-opted into tissue-specific expression pattern or whether the evolutionary rates have increased after the expression patterns have changed.…”

Section: Stability Of Expression Patternmentioning

confidence: 99%

Evolutionary constraints shape caste-specific gene expression across 15 ant species

et al. 2017

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Development of polymorphic phenotypes from similar genomes requires gene expression differences. However, little is known about how morph-specific gene expression patterns vary on a broad phylogenetic scale. We hypothesize that evolution of morph-specific gene expression, and consequently morph-specific phenotypic evolution, may be constrained by gene essentiality and the amount of pleiotropic constraints. Here, we use comparative transcriptomics of queen and worker morphs, that is, castes, from 15 ant species to understand the constraints of morph-biased gene expression. In particular, we investigate how measures of evolutionary constraints at the sequence level (expression level, connectivity, and number of gene ontology [GO] terms) correlate with morph-biased expression. Our results show that genes indeed vary in their potential to become morph-biased. The existence of genes that are constrained in becoming caste-biased potentially limits the evolutionary decoupling of the caste phenotypes, that is, it might result in "caste load" occasioning from antagonistic fitness variation, similarly to sexually antagonistic fitness variation between males and females. On the other hand, we suggest that genes under low constraints are released from antagonistic variation and thus more likely to be co-opted for morph specific use. Overall, our results suggest that the factors that affect sequence evolutionary rates and evolution of plastic expression may largely overlap.

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An Organismal Perspective on the Evolution of Insect Societies

Cited by 28 publications

References 108 publications

Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation

Superorganismality and caste differentiation as points of no return: how the major evolutionary transitions were lost in translation

Sex allocation conflict and sexual selection throughout the lifespan of eusocial colonies

Evolutionary constraints shape caste-specific gene expression across 15 ant species

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