Genes and genomic processes underpinning the social lives of ants

Favreau, Emeline; Martínez-Ruiz, Carlos; Santiago, Leandro Rodrigues; Hammond, Robert L.; Wurm, Yannick

doi:10.1016/j.cois.2017.12.001

Cited by 27 publications

(19 citation statements)

References 78 publications

(21 reference statements)

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“…Such proteins help pigment transport and vision in D. melanogaster and the butterfly Papilio xuthus ( Pelosi et al, 2018 ). In sum, all three candidate genes have putative functions related to environmental perception, in line with the complex social phenotype requiring subtle changes in environmental perception or signaling ( Favreau et al, 2018 ).…”

Section: Discussionmentioning

confidence: 96%

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Martínez-Ruiz

Pracana

Stolle

et al. 2020

eLife

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Supergene regions maintain alleles of multiple genes in tight linkage through suppressed recombination. Despite their importance in determining complex phenotypes, our empirical understanding of early supergene evolution is limited. Here we focus on the young "social" supergene of fire ants, a powerful system for disentangling the effects of evolutionary antagonism and suppressed recombination. We hypothesize that gene degeneration and social antagonism shaped the evolution of the fire ant supergene, resulting in distinct patterns of gene expression. We test these ideas by identifying allelic differences between supergene variants, characterizing allelic expression across populations, castes and body parts, and contrasting allelic expression biases with differences in expression between social forms. We find strong signatures of gene degeneration and gene-specific dosage compensation. On this background, a small portion of the genes has the signature of adaptive responses to evolutionary antagonism between social forms.

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Section: Discussionmentioning

confidence: 96%

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Martínez-Ruiz

Pracana

Stolle

et al. 2020

eLife

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“…The Reproductive Groundplan Hypothesis 12,65,117 (& other Toolkit-like hypotheses 118 ) posits that the seasonally-oscillating ecological demands lead to phenotypic plasticity of the ancestral Ur-ant (between forager-like and queen-like states). This evolutionary history is reflected today by the partitioned expression of the same genome between workers and queens 29,119,120 . This plastic state is still observed in species considered to be "facultatively social" (note that this label does not imply that all social species progress along similar or predictable evolutionary paths 18 122 , control of nutritional intake 123 , and multiple modes of physical interaction such as piping and drumming 124 .…”

Section: Eusocial Colony Physiology: Hormonal Mechanisms and Evolutiomentioning

confidence: 99%

“…First, the epigenetic plasticity of eusocial insect workers situates them as tractable models to disentangle genetic and environmental influences on behavior 88,163 . 29,120,146,155,164 .…”

Section: Future Directions and Questionsmentioning

confidence: 99%

Distributed physiology and the molecular basis of social life in eusocial insects

Friedman

Johnson

Linksvayer

2020

Hormones and Behavior

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The traditional focus of physiological and functional genomic research is on molecular processes that play out within a single body. In contrast, when social interactions occur, molecular and behavioral responses in interacting individuals can lead to physiological processes that are distributed across multiple individuals. In eusocial insect colonies, such multi-body processes are tightly integrated, involving social communication mechanisms that regulate the physiology of colony members. As a result, conserved physiological mechanisms, for example related to pheromone detection and neural signaling pathways, are deployed in novel contexts and regulate emergent colony traits during the evolutionary origin and elaboration of social complexity. Here we review conceptual frameworks for organismal and colony physiology, and highlight functional genomic, physiological, and behavioral research exploring how colony-level traits arise from physical and chemical interactions among nestmates. We highlight mechanistic work exploring how colony traits arise from physical and chemical interactions among physiologically-specialized nestmates of 1 various developmental stages. We consider similarities and differences between organismal and colony physiology, and make specific predictions based on a decentralized perspective on the function and evolution of colony traits. Integrated models of colony physiological function will be useful to address fundamental questions related to the evolution and ecology of collective behavior in natural systems. Colony Organization = Social Anatomy + Social PhysiologyEusocial colonial insects, such as ants, termites, and honey bees, thrive across almost all terrestrial ecosystems 1,2 . The ecological success of these species rests in their use of colony traits, such as nest architecture 3,4 and collective foraging behavior 5-7 , which are functionally absent in solitary insects yet keenly developed in eusocial taxa. In the eusocial insects, division of labor (DOL) describes how nestmates vary in their form and function. DOL formalizes the extent of specialization among nestmates in the performance of tasks, usually with a physiological or morphological basis or arising from nestmate age (temporal polyethism) and experience [8][9][10][11] . We build off of the conceptual framework of Johnson & Linksvayer 12 that considers eusocial colony organization from the perspective of social anatomy & social physiology : Social anatomy is the notion that colonies are composed of specialized parts with limited roles, like the organs of an individual animal. Specialized colony anatomy allows for greater productivity and efficiency for the completion of many tasks.Physiological specialization exists at multiple levels within the colony. Queen-worker specialization allows for an increased reproductive output of queens alongside increased work output from workers, from the same diploid female genome 13 .Subspecialization among workers can manifest as permanent variation in body morphology 14 , temporal polyet...

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“…Ants are a globally distributed clade of social insect species ( Gibb et al., 2017 , Parr et al., 2017 , Ward, 2014 ), and ecological factors shape the evolution of ant collective behavior ( Gordon, 2013 , Gordon, 2014 , Lanan, 2014 ). Rapid advances in high-throughput sequencing technologies are providing insight into the genomic, transcriptomic, and epigenomic differences among social insect species ( Boomsma et al., 2017 , Favreau et al., 2018 , Toth and Rehan, 2017 ). Molecular studies have characterized various mechanistic aspects of division of labor among workers within social insect colonies ( Friedman and Gordon, 2016 , Kamhi and Traniello, 2013 , Linksvayer, 2015 , Simola et al., 2016 ), building on a long history of diverse research into social insect behavior ( Detrain and Deneubourg, 2006 , Gordon, 1992 , Hölldobler and Wilson, 2009 , Seeley, 2010 , von Frisch, 1974 ).…”

Section: Introductionmentioning

confidence: 99%

The Role of Dopamine in the Collective Regulation of Foraging in Harvester Ants

et al. 2018

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SummaryColonies of the red harvester ant (Pogonomyrmex barbatus) differ in how they regulate collective foraging activity in response to changes in humidity. We used transcriptomic, physiological, and pharmacological experiments to investigate the molecular basis of this ecologically important variation in collective behavior among colonies. RNA sequencing of forager brain tissue showed an association between colony foraging activity and differential expression of transcripts related to biogenic amine and neurohormonal metabolism and signaling. In field experiments, pharmacological increases in forager brain dopamine titer caused significant increases in foraging activity. Colonies that were naturally most sensitive to humidity were significantly more responsive to the stimulatory effect of exogenous dopamine. In addition, forager brain tissue significantly varied among colonies in biogenic amine content. Neurophysiological variation among colonies associated with individual forager sensitivity to humidity may reflect the heritable molecular variation on which natural selection acts to shape the collective regulation of foraging.

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Genes and genomic processes underpinning the social lives of ants

Cited by 27 publications

References 78 publications

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Genomic architecture and evolutionary antagonism drive allelic expression bias in the social supergene of red fire ants

Distributed physiology and the molecular basis of social life in eusocial insects

The Role of Dopamine in the Collective Regulation of Foraging in Harvester Ants

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