Insects with similar social complexity show convergent patterns of adaptive molecular evolution

Dogantzis, Kathleen A.; Harpur, Brock A.; Rodrigues, André; Beani, L.; Toth, Amy L.; Zayed, Amro

doi:10.1038/s41598-018-28489-5

Cited by 24 publications

(28 citation statements)

References 57 publications

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“…Second, we found significant enrichment of caste-biased genes among those under positive selection in a McDonald-Kreitman test (25% of genes under positive selection are caste-biased, hypergeometric test: P = 0.03). Most of these genes (65%) were up-regulated in queen versus worker abdomens, and include genes that function in reproduction in honey bees (e.g., orthologs of the Drosophila melanogaster genes notch and yolkless), indicating that reproductive function is likely under strong selection, as shown for other eusocial bees with a solitary phase prior to the emergence of workers (60,66).…”

Section: Plasticity Of Developmental Gene Expression Is Predictive Ofmentioning

confidence: 90%

Developmental plasticity shapes social traits and selection in a facultatively eusocial bee

Kapheim

Jones

Pan

et al. 2020

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

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Developmental plasticity generates phenotypic variation, but how it contributes to evolutionary change is unclear. Phenotypes of individuals in caste-based (eusocial) societies are particularly sensitive to developmental processes, and the evolutionary origins of eusociality may be rooted in developmental plasticity of ancestral forms. We used an integrative genomics approach to evaluate the relationships among developmental plasticity, molecular evolution, and social behavior in a bee species (Megalopta genalis) that expresses flexible sociality, and thus provides a window into the factors that may have been important at the evolutionary origins of eusociality. We find that differences in social behavior are derived from genes that also regulate sex differentiation and metamorphosis. Positive selection on social traits is influenced by the function of these genes in development. We further identify evidence that social polyphenisms may become encoded in the genome via genetic changes in regulatory regions, specifically in transcription factor binding sites. Taken together, our results provide evidence that developmental plasticity provides the substrate for evolutionary novelty and shapes the selective landscape for molecular evolution in a major evolutionary innovation: Eusociality.

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Section: Plasticity Of Developmental Gene Expression Is Predictive Ofmentioning

confidence: 90%

Developmental plasticity shapes social traits and selection in a facultatively eusocial bee

Kapheim

Jones

Pan

et al. 2020

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

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“…Finally, we performed pairwise Fisher's exact tests of overlap between these directional gene lists in comparison to the shared background list. This test is commonly used in examinations of the intersection between gene lists (e.g., Amsalem et al, ; Dogantzis et al, ; Rutter et al, ) to determine whether the degree of overlap is greater than might be predicted under a null model. All reported results were significant at an FDR‐corrected p < .05.…”

Section: Methodsmentioning

confidence: 99%

Transcriptome analysis reveals nutrition‐ and age‐related patterns of gene expression in the fat body of pre‐overwintering bumble bee queens

et al. 2020

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Many diapausing insects undergo a nutrient storage period prior to their entry into diapause. Bumble bee queens diapause as adults in the winter preceding their spring nest initiation period. Before diapause, they sequester glycogen and lipids, which they metabolize during the overwintering period. We used RNA sequencing to examine how age and nectar diet (specifically, the concentration of sucrose in nectar) impact gene expression in the pre‐overwintering bumble bee queen fat body, the “liver‐like” organ in insects with broad functions related to nutrient storage and metabolism. We found that diet on its own, and in combination with age, impacts the expression of genes involved in detoxification. Age was also a strong driver of gene expression, especially at earlier ages (up to 3 days). In addition to these molecular correlates of diet and age, we also found a putative molecular signature of diapause entry or preparation in adult queens in the oldest age group (12 days) fed the most sucrose‐rich diet, based on comparisons between our data set and another transcriptome data set from bumble bee queens. This transcriptomic pattern suggests that preparation for (or entry into) diapause might be in part mediated by nutritional state in bumble bee queens. Collectively, these findings show that there are molecular processes in the fat body that are responsive to sucrose levels in the diet and/or associated with age‐related maturational changes. A better understanding of these processes may shed light on important aspects of bumble bee biology, such as queen responses to nutritional and other forms of stress, and the factors that regulate their entrance into diapause.

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“…The simplest societies in our study are represented by Mischocyttarus basimacula basimacula (Cameron) and Polistes canadensis; wasps in these two genera are all independent nest founders and lack morphological castes (defined as allometric differences in body shape, rather than overall size) or any documented form of lifetime caste-role commitment [48][49][50][51] . They live in small family groups of reproductively totipotent females, one of whom usually dominates reproduction (the queen); if the queen dies she is succeeded by a previously-working individual 21 . As such, these societies represent some of the earliest stages in the major transition, where caste roles are least well defined, and where individual-level plasticity is advantageous for maximising inclusive fitness.…”

Section: Study Speciesmentioning

confidence: 99%

“…The copyright holder for this this version posted December 10, 2020. ; https://doi.org/10.1101/2020.12.08.407056 doi: bioRxiv preprint 4 studies have suggested that the processes regulating different levels of social complexity may be different 17,19,21 . The innovations in social complexity and the shift in the unit of selection (from individual-to group-level 22 ) that accompany the major transition may therefore be accompanied by genomic evolution, throwing into question whether a universal conserved genomic toolkit regulates social behaviours across the spectrum of the major transition 8 .…”

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confidence: 99%

Genetic toolkit for sociality predicts castes across the spectrum of social complexity in wasps

Wyatt

Bentley

Taylor

et al. 2020

Preprint

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Major evolutionary transitions describe how biological complexity arises; e.g. in evolution of complex multicellular bodies, and superorganismal insect societies. Such transitions involve the evolution of division of labour, e.g. as queen and worker castes in insect societies. Castes across different evolutionary lineages are thought to be regulated by a conserved genetic toolkit. However, this hypothesis has not been tested thoroughly across the complexity spectrum of the major transition. Here we reveal, using machine learning analyses of brain transcription, evidence of a shared genetic toolkit across the spectrum of social complexity in Vespid wasps. Whilst molecular processes underpinning the simpler societies (which likely represent the origins of social living) are conserved throughout the major transition, additional processes appear to come into play in more complex societies. Such fundamental shifts in regulatory processes with complexity may typify other major evolutionary transitions, such as the evolution of multicellularity.

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Insects with similar social complexity show convergent patterns of adaptive molecular evolution

Cited by 24 publications

References 57 publications

Developmental plasticity shapes social traits and selection in a facultatively eusocial bee

Developmental plasticity shapes social traits and selection in a facultatively eusocial bee

Transcriptome analysis reveals nutrition‐ and age‐related patterns of gene expression in the fat body of pre‐overwintering bumble bee queens

Genetic toolkit for sociality predicts castes across the spectrum of social complexity in wasps

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