Climbing the social ladder: the molecular evolution of sociality

Rehan, Sandra M.; Toth, Amy L.

doi:10.1016/j.tree.2015.05.004

Cited by 152 publications

(197 citation statements)

References 73 publications

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“…There is a debate over the relative roles for core sets of conserved genes (42-48) and taxon-restricted genes (TRGs) (5,44,47,49,50) in the evolution of convergent phenotypes (7,44,46). We found evidence that both types of gene classes play peripheral roles in the molecular networks associated with phenotypic differentiation in our study species.…”

Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 63%

“…However, genome sequence alone is not sufficient to explain diverse phenotypic variation because such analyses infer associations based on gene evolution and gene sharing rather than directly identifying differentially expressed genes (DEGs) in the phenotypes of interest (7). Here, in addition to genome and microRNA (miRNA) sequencing, we use deep transcriptome and methylome sequencing of single brains from alternative phenotypes to determine the differential molecular processes associated with highly plastic phenotypes in two species of eusocial insects (8).…”

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confidence: 99%

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Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

190

276

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Phenotypic plasticity is important in adaptation and shapes the evolution of organisms. However, we understand little about what aspects of the genome are important in facilitating plasticity. Eusocial insect societies produce plastic phenotypes from the same genome, as reproductives (queens) and nonreproductives (workers). The greatest plasticity is found in the simple eusocial insect societies in which individuals retain the ability to switch between reproductive and nonreproductive phenotypes as adults. We lack comprehensive data on the molecular basis of plastic phenotypes. Here, we sequenced genomes, microRNAs (miRNAs), and multiple transcriptomes and methylomes from individual brains in a wasp (Polistes canadensis) and an ant (Dinoponera quadriceps) that live in simple eusocial societies. In both species, we found few differences between phenotypes at the transcriptional level, with little functional specialization, and no evidence that phenotype-specific gene expression is driven by DNA methylation or miRNAs. Instead, phenotypic differentiation was defined more subtly by nonrandom transcriptional network organization, with roles in these networks for both conserved and taxon-restricted genes. The general lack of highly methylated regions or methylome patterning in both species may be an important mechanism for achieving plasticity among phenotypes during adulthood. These findings define previously unidentified hypotheses on the genomic processes that facilitate plasticity and suggest that the molecular hallmarks of social behavior are likely to differ with the level of social complexity.

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Section: Role For Conserved Toolkit Genes and Taxon-restricted Genes Inmentioning

confidence: 63%

mentioning

confidence: 99%

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Patalano

Vlasova

Wyatt

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

190

276

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“…6). The conspicuous response from the fly to honeybee pheromone may, therefore, lie in conserved olfactory or other30 signaling mechanisms that remain linked to female fecundity and ovary de-activation, as predicted by socio-evolutionary hypotheses24313233. Or98a and HOB may indeed be linked to reproduction: the former mediates female fly mating behaviour34 and the latter molecule varies in its expression as a function of reproductive caste across Apis spp 35…”

Section: Resultsmentioning

confidence: 99%

A novel screen for genes associated with pheromone-induced sterility

Camiletti

Percival‐Smith

Croft

et al. 2016

Sci Rep

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For honey bee and other social insect colonies the ‘queen substance’ regulates colony reproduction rendering workers functionally sterile. The evolution of worker reproductive altruism is explained by inclusive fitness theory, but little is known of the genes involved or how they regulate the phenotypic expression of altruism. We previously showed that application of honeybee queen pheromone to virgin fruit flies suppresses fecundity. Here we exploit this finding to identify genes associated with the perception of an ovary-inhibiting social pheromone. Mutational and RNAi approaches in Drosophila reveal that the olfactory co-factor Orco together with receptors Or49b, Or56a and Or98a are potentially involved in the perception of queen pheromone and the suppression of fecundity. One of these, Or98a, is known to mediate female fly mating behaviour, and its predicted ligand is structurally similar to a methyl component of the queen pheromone. Our novel approach to finding genes associated with pheromone-induced sterility implies conserved reproductive regulation between social and pre-social orders, and further helps to identify candidate orthologues from the pheromone-responsive pathway that may regulate honeybee worker sterility.

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“…Yanega 1997; Field et al 2010, 2012; Kapheim et al 2012, 2015a; Kocher et al 2013; Rehan and Toth 2015), and investigating these mechanisms requires taxa that straddle this transition (Field et al 2010; Rehan and Toth 2015). Socially polymorphic sweat bees (Hymenoptera: Halictidae) are ideal models for this purpose, because different populations of the same species exhibit either eusocial or solitary behaviour (Soucy and Danforth 2002; Chapuisat 2010).…”

Section: Introductionmentioning

confidence: 99%

Limited social plasticity in the socially polymorphic sweat bee Lasioglossum calceatum

Davison

Field

2018

Behav Ecol Sociobiol

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Eusociality is characterised by a reproductive division of labour, where some individuals forgo direct reproduction to instead help raise kin. Socially polymorphic sweat bees are ideal models for addressing the mechanisms underlying the transition from solitary living to eusociality, because different individuals in the same species can express either eusocial or solitary behaviour. A key question is whether alternative social phenotypes represent environmentally induced plasticity or predominantly genetic differentiation between populations. In this paper, we focus on the sweat bee Lasioglossum calceatum, in which northern or high-altitude populations are solitary, whereas more southern or low-altitude populations are typically eusocial. To test whether social phenotype responds to local environmental cues, we transplanted adult females from a solitary, northern population, to a southern site where native bees are typically eusocial. Nearly all native nests were eusocial, with foundresses producing small first brood (B1) females that became workers. In contrast, nine out of ten nests initiated by transplanted bees were solitary, producing female offspring that were the same size as the foundress and entered directly into hibernation. Only one of these ten nests became eusocial. Social phenotype was unlikely to be related to temperature experienced by nest foundresses when provisioning B1 offspring, or by B1 emergence time, both previously implicated in social plasticity seen in two other socially polymorphic sweat bees. Our results suggest that social polymorphism in L. calceatum predominantly reflects genetic differentiation between populations, and that plasticity is in the process of being lost by bees in northern populations.Significance statementPhenotypic plasticity is thought to play a key role in the early stages of the transition from solitary to eusocial behaviour, but may then be lost if environmental conditions become less variable. Socially polymorphic sweat bees exhibit either solitary or eusocial behaviour in different geographic populations, depending on the length of the nesting season. We tested for plasticity in the socially polymorphic sweat bee Lasioglossum calceatum by transplanting nest foundresses from a northern, non-eusocial population to a southern, eusocial population. Plasticity would be detected if transplanted bees exhibited eusocial behaviour. We found that while native bees were eusocial, 90% of transplanted bees and their offspring did not exhibit traits associated with eusociality. Environmental variables such as time of offspring emergence or temperatures experienced by foundresses during provisioning could not explain these differences. Our results suggest that the ability of transplanted bees to express eusociality is being lost, and that social polymorphism predominantly reflects genetic differences between populations.Electronic supplementary materialThe online version of this article (10.1007/s00265-018-2475-9) contains supplementary material, which is available t...

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Climbing the social ladder: the molecular evolution of sociality

Cited by 152 publications

References 73 publications

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

A novel screen for genes associated with pheromone-induced sterility

Limited social plasticity in the socially polymorphic sweat bee Lasioglossum calceatum

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