American Society of Naturalists

Zachary I. Phillips (Jan 2021)

A miniature cockroach hitchhikes twice on its journey between host ant colonies, bypassing vulnerable young colonies

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Each spring after the rains arrive in Texas, cockroaches mount winged ants at daybreak and ride them across the sky. Where are the cockroaches going? The author, bless his heart, once thought this would be a straightforward question to address in his dissertation.

Attaphila fungicola, a miniature cockroach that lives with leaf-cutter ant colonies and their mutualist fungal gardens, hitchhikes on female alates (winged queens) during colony nuptial flights. The roach’s only available host in the region is the Texas leaf-cutter ant (Atta texana), and hitchhiking on female alates suggests that the roach is vertically transmitted from leaf-cutter parent colony to daughter colony, remaining with female alates as they transition into queens founding new nests; however, leaf-cutter queens initiating colonies have few resources and extremely high mortality rates. As a consequence, vertical transmission could tether roaches to vulnerable hosts likely to die.

Drawing from principles of disease ecology, the author proposes that roaches have evolved an alternative mode of horizontal transmission: Instead of remaining with new queens, roaches use female alates as dispersal agents to reach already established colonies. In its general form, this mode of transmission might be used by a variety of symbionts (parasites, mutualists and commensals) to co-disperse with host propagules and, following dispersal, to avoid infecting low quality early stages of host development.

To test this hypothesis, the author conducted behavioral assays in the field. The results indicate that roaches abandon female alates after nuptial flights, bypass early stages of colony development, and can use a sequence of two hitchhiking steps to disperse between established colonies. First, the roaches can ride female alates to emigrate from upstream host colonies, and second, the roaches can ride leaves carried by foragers to infect downstream host colonies.

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Abstract

Symbionts of ant colonies can hitchhike on winged ant reproductives (alates) during colony nuptial flights. Attaphila fungicola Wheeler, a miniature cockroach that lives in the nests of Texas leaf-cutter ants (Atta texana Buckley), hitchhikes on female alates (winged queens). Hitchhiking roaches are presumably vertically transmitted from leaf-cutter parent colony to daughter colony, remaining with female alates as they transition into foundresses (workerless queens); however, foundresses have limited resources and high mortality rates. Rather than remaining with foundresses likely to die (vertical transmission), roaches might abandon them during dispersal to infect higher quality later stages of colony development (female alate-vectored transmission). In field experiments, I find evidence for female alate-vectored transmission, and discover roaches use a second hitchhiking step, riding foraged plant material, to infect established colonies. This work reveals a novel relationship between host dispersal and symbiont transmission, and shows colony development can be an important selection pressure on transmission.