Ant Genetics: Reproductive Physiology, Worker Morphology, and Behavior

Abstract

Many exciting studies have begun to elucidate the genetics of the morphological and physiological diversity of ants, but as yet few studies have investigated the genetics of ant behavior directly. Ant genomes are marked by extreme rates of gene turnover, especially in gene families related to olfactory communication, such as the synthesis of cuticular hydrocarbons and the perception of environmental semiochemicals. Transcriptomic and epigenetic differences are apparent between reproductive and sterile females, males and females, and workers that differ in body size. Quantitative genetic approaches suggest heritability of task performance, and population genetic studies indicate a genetic association with reproductive status in some species. Gene expression is associated with behavior including foraging, response to queens attempting to join a colony, circadian patterns of task performance, and age-related changes of task. Ant behavioral genetics needs further investigation of the feedback between individual-level physiological changes and socially mediated responses to environmental conditions.

Ant collective behavior is heritable and shaped by selection

“…Given that trait variation must be heritable in order for the trait to respond to selection and evolve over time, quantifying heritability is the crucial first step in studying trait evolution (Falconer & Mackay 1996;Lynch & Walsh 1998). Previous studies in ants, honey bees, and sticklebacks suggest that collective behaviors and other group-level traits are heritable (Linksvayer 2006;Hunt et al 2007;Wark et al 2011;Greenwood et al 2015;Friedman & Gordon 2016). Additionally, candidate gene studies have linked allelic variation to variation in collective behavior, providing further evidence that collective behavior is heritable (Krieger 2005;Wang et al 2008;Wang et al 2013;Tang et al 2018).…”

“…However, despite this long-term intense interest in the evolution of colony-level traits, we still know empirically very little about the key parameters governing the evolution of these traits. Indeed, while recent molecular studies have begun to characterize the genomic, transcriptomic, and epigenetic differences between species, between castes within a species, and between individual workers (Friedman & Gordon 2016;Gospocic et al 2017;Warner et al 2017;Chandra et al 2018;Walsh et al 2018), little is known about the genetic architecture of collective behavior, caste ratio, and sex ratio (Linksvayer 2006). Similarly, while it is clear that colony-level phenotypes can be shaped by patterns of selection within-and between-colonies (Owen 1986;Moritz 1989;Ratnieks & Reeve 1992;Tsuji 1994Tsuji , 1995Banschbach & Herbers 1996;Tarpy et al 2004), few studies have attempted to empirically quantify patterns of selection acting on social insect traits.…”

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

“…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 .…”

“…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 .…”

Molecular insights into the pathways underlying naked mole-rat eusociality

“…The original definition, derived from studies of social insects, requires three criteria: a reproductive division of labour, overlapping generations, and cooperative care of young [3, 4], although it has been argued that physically distinct morphological castes should also be present [5]. This extraordinary cooperative way of life is famously observed in invertebrates, such as the social hymenoptera, but also other diverse groups such as crustaceans, and more recently, some mammals (6–9). The importance of eusociality as a strategy is exemplified by the fact that eusocial species may constitute 75% of the insect biomass in some ecosystems [10, 11].…”