A symbiotic aphid selfishly manipulates attending ants via dopamine in honeydew

Tatsumi Kudo,Eisuke Hasegawa,Hitoshi Aonuma

doi:10.1038/s41598-021-97666-w

Tatsumi Kudo, Eisuke Hasegawa + Show 1 more

Open Access

https://doi.org/10.1038/s41598-021-97666-w

Copy DOI

Journal: Scientific Reports	Publication Date: Sep 17, 2021
Citations: 6	License type: open-access

Affiliation: Hokkaido University, Kobe University

Abstract

Symbiotic relationships are widespread in nature, but the mechanisms maintaining these relationships remain to be elucidated because symbiosis incurs a maintenance cost to each participant, which lowers its reproductive rate. In host-parasite relationships, parasites are known to manipulate the host's behavior selfishly, and there is an arms race between them. Selfish manipulations also occur in symbiosis, but the effects of selfish manipulations on symbiosis are not fully understood. Here, we show that an ant-associated aphid manipulates attending ants to receive stronger protection. Aphid honeydew regurgitated by ants contains dopamine (DA). The ants showed low aggressiveness before contact with the aphids, but it rose after contact. Administration of DA to the ants increased ant aggressiveness as the concentration increased, while an antagonist of DA inhibited this effect. The other 3 amines showed no effect on aggressiveness. A previous study showed that attending ants selfishly manipulate aphids by increasing the reproductive rate of green morph to obtain high-quality honeydew. These results suggest that mutual selfish manipulation benefits both participants and is likely to strengthen symbiosis. The selfishness of each participant may contribute to sustaining this symbiosis because their selfishness increases their long-term fitness.

Highlights

Symbiotic relationships are widespread in nature, but the mechanisms maintaining these relationships remain to be elucidated because symbiosis incurs a maintenance cost to each participant, which lowers its reproductive rate
Amazing biodiversity is found in nature[1], and how and why it is maintained is one of the most important issues in ecology and evolutionary b iology[2]
Under natural selection, symbiotic relationships are predicted to decay because the cost necessary to maintain the relationship lowers the instantaneous reproductive rate (= arithmetic mean fitness)[3]

Summary

Introduction

Symbiotic relationships are widespread in nature, but the mechanisms maintaining these relationships remain to be elucidated because symbiosis incurs a maintenance cost to each participant, which lowers its reproductive rate. A previous study showed that attending ants selfishly manipulate aphids by increasing the reproductive rate of green morph to obtain high-quality honeydew. These results suggest that mutual selfish manipulation benefits both participants and is likely to strengthen symbiosis. Under natural selection, symbiotic relationships are predicted to decay because the cost necessary to maintain the relationship lowers the instantaneous reproductive rate (= arithmetic mean fitness)[3]. Mutual selfish manipulations can increase mutual dependency because such manipulations increase benefits of participants from the symbiotic system In such case, selfish manipulations may be accepted by a partner in symbiosis[6,13]. Selfish manipulation by the host is beneficial to both participants, and this manipulation is acceptable to the ants[6]

Objectives

Methods

Results

Conclusion