Maternal and nourishment factors interact to influence offspring developmental trajectories in social wasps

Abstract

The social and nutritional environments during early development have the potential to affect offspring traits, but the mechanisms and molecular underpinnings of these effects remain elusive. We used Polistes fuscatus paper wasps to dissect how maternally controlled factors (vibrational signals and nourishment) interact to induce different caste developmental trajectories in female offspring, leading to worker or reproductive (gyne) traits. We established a set of caste phenotype biomarkers in P. fuscatus females, finding that gyne-destined individuals had high expression of three caste-related genes hypothesized to have roles in diapause and mitochondrial metabolism. We then experimentally manipulated maternal vibrational signals (via artificial 'antennal drumming') and nourishment levels (via restricted foraging). We found that these caste-related biomarker genes were responsive to drumming, nourishment level or their interaction. Our results provide a striking example of the potent influence of maternal and nutritional effects in influencing transcriptional activity and developmental outcomes in offspring. RightsWorks produced by employees of the U.S. Government as part of their official duties are not copyrighted within the U.S. The content of this document is not copyrighted. The social and nutritional environments during early development have the potential to affect offspring traits, but the mechanisms and molecular underpinnings of these effects remain elusive. We used Polistes fuscatus paper wasps to dissect how maternally controlled factors (vibrational signals and nourishment) interact to induce different caste developmental trajectories in female offspring, leading to worker or reproductive (gyne) traits. We established a set of caste phenotype biomarkers in P. fuscatus females, finding that gyne-destined individuals had high expression of three caste-related genes hypothesized to have roles in diapause and mitochondrial metabolism. We then experimentally manipulated maternal vibrational signals (via artificial 'antennal drumming') and nourishment levels (via restricted foraging). We found that these caste-related biomarker genes were responsive to drumming, nourishment level or their interaction. Our results provide a striking example of the potent influence of maternal and nutritional effects in influencing transcriptional activity and developmental outcomes in offspring.

Care-giver identity impacts offspring development and performance in an annually social bumble bee

“…Evidence for maternal manipulation has been found in a number of insect lineages, including weakly or flexibly social bees [ 53 – 56 ], and in many vertebrate species [e.g., 57,58]. In eusocial insects, maternal manipulation theory has been extended to include caste bias, such that in the systems with both maternal and alloparental care, queens are predicted to rear offspring that are more likely to develop into sterile workers versus reproductive queens [ 59 ]. This extension of maternal manipulation theory was developed because eusocial insect workers do not require manipulation to remain as helpers in the nest, but development into a queen might allow an individual to leave and initiate a new nest.…”

Emergence of cooperation and division of labor in the primitively eusocial waspRopalidia marginata

“…Age-or morphology-based nonreproductive DOL has been reported mostly in colonies of eusocial species and very rarely in other forms of social organizations (15). However, parental manipulation of resources provided to offspring (16) and "maternal vibrational signals" by antennal drumming have been reported to increase the probability of larvae developing into subordinate (worker) adults (17)(18)(19). Communal species, which are considered to be a transitional step in the evolution of eusocial insects from their solitary counterparts, do not display reproductive or nonreproductive DOL (2,20).…”

Adult-larvae vibrational communication in paper wasps: the role of abdominal wagging inPolistes dominula

“…However, according to Brillet et al (1999) and Jeanne (2009), the substrate-borne vibrations produced by the oscillatory movements in Polistes wasps could be seen as signals that advertise the presence of a dominant and breeding individual on the nest, to both maintain hierarchy on the nest and prepare the larvae for their future status as workers. In this way, vibrations could trigger physiological events in larvae driving caste development toward a worker phenotype, as has been demonstrated in P. fuscatus with antennal drumming (Suryanarayanan et al, 2011b;Jandt et al, 2017). We did not test long-term effects, but this hypothesis might explain why AbW is more common in dominant than in subordinate individuals and why it is more frequent in the early than in the late phase of the colony cycle (Savoyard et al, 1998;Brillet et al, 1999;Jeanne, 2009).…”

“…The playback of vibrations previously recorded on a substrate allows researchers to switch from correlational evidence to a direct test of signal function of the recorded vibrations, and thus to assess the identity of the receivers as well as the function of the signal. Indeed, the first steps toward this direction recently started to transform our understanding of intracolonial communication in insect societies (Evans et al, 2007;Suryanarayanan et al, 2011a,b;Hager and Kirchner, 2014;Jandt et al, 2017).…”

“…The idea is that vibrations would interfere with the developmental pathway of larvae, which would be biased toward the worker phenotype (Jeanne, 2009;Mignini and Lorenzi, 2015). The vibration effect on the phenotype has been recently demonstrated for P. fuscatus, in which AD on cell rims produces vibrations that interfere with the food pathway to bias larval fate toward a worker phenotype (Suryanarayanan et al, 2011a;Jandt et al, 2017).…”