Ant‐induced evolutionary patterns in aphids

Abstract

This review investigates ant–aphid mutualism (trophobiosis), in particular focusing on evolutionary processes in aphids resulting from this interaction. This broad literature review allows us to revise existing views on certain aspects of this mutualism and provide the first timeline of its possible development over a geological timescale. We propose a new classification of ant–aphid mutualism with respect to its ecological characteristics and present new explanations of the development of certain morphological structures of aphids as resulting from adaptation to a trophobiotic relationship with ants. In light of these findings, the presence of the so‐called ‘trophobiotic organ’ in all myrmecophilous aphids is questioned. We review various communication modes between aphids and mutualistic ants and the possible influence of this symbiosis on modifications of aphid life cycles. Recent evidence on the suspected role of endosymbiotic bacteria in the development of mutualism is discussed. Finally, we propose a first timeline of ant–aphid interactions leading to the development of particular adaptations of aphids to mutualism, from general interactions between diverging Aphidomorpha and ants in the late Mesozoic to more specific coevolution between the aphid tribe Fordini and the ant genus Lasius.

A trail pheromone mediates the mutualism between ants and aphids

“…This interpretation is in line with the fact that many ant-aphid associations show a flexibility in partner choice. 59 When a better partner is found, the responses to its signals, which are common and can be easily perceived, will be quickly strengthened, leading to a shift between mutualistic partners. Reproduction of aphids has previously been shown to be either positively or negatively influenced by ant attendance.…”

Seasonal changes in cuticular hydrocarbons in response to polyphenism in the host‐alternating aphid Prociphilus oriens

“…The secreted wax is hydrophobic and can protect aphids from contamination of honeydew and provide some protection against enemies and unfavorable environmental conditions (Smith 1999;Pike et al 2002;Moss et al 2006;Ammar et al 2013;Kasahara et al 2019;Depa et al 2020). However, there should be fitness costs to the production of external waxes (Pope 1983).…”

Drop when the stakes are high: adaptive, flexible use of dropping behaviour by aphids

“…Some aphids also possess defensive structures such as frontal horns that can be used to attack predators (Arakaki, 1989;Pickett et al, 2007). Indirect defence also occurs for some aphids -myrmecophilous species form mutualisms with ants, which deter predators, and consequently exhibit reduced predator-avoidance behaviours (Depa et al, 2020). The deployment of behavioural defences can be more flexible, however, in response to the context of predation than morphological adaptations and indirect defences, and so the trade-offs associated with dropping will most valuably be weighed-up relative to alternative defensive behaviours.…”