Alternative adaptations, sympatric speciation and the evolution of parasitic, inquiline ants

Inquiline ant species are workerless social parasites whose queens reproduce in colonies of other species alongside the host queens. Inquilines arise either when one non-parasitic species evolves into an inquiline parasite of another non-parasitic species (the interspecific hypothesis), or by the speciation of intraspecific inquilines from their host stock (the intraspecific hypothesis): it is unlikely that inquilines evolve from other forms of social parasite. This paper reviews the evidence for and against the inter-and intraspecific hypotheses. All inquilines are close phylogenetic relatives of their host species (loose ‘Emery's rule’), and some are their host's closest relative (strict ‘Emery's rule’). A problem for the interspecific hypothesis is how to explain the strict Emery's rule, because phylogenetic constraints on host choice are probably quite weak. By contrast, the intraspecific hypothesis has difficulty accounting for the parasites' sympatric reproductive isolation.

Facultative polygyny, in which queens may found colonies alone or by adoption into an existing multi-queen colony, should promote the evolution of small intraspecific inquilines. This is because small colony-founding queens should preferentially seek adoption, which provides the opportunity to produce a sexual-only brood. We suggest that microgynes, i.e. miniature queens found in some polygynous ants, represent such parasites. We review the evidence that inquiline species have evolved intraspecifically from microgynes in Myrmica ants. The coexistence within a species of a monogynous (singly-queened) and a polygynous form is probably a phenomenon usually unconnected with inquiline evolution.

The reproductive isolation of intraspecific inquilines plausibly arises from divergent breeding behaviour associated with the parasites' small size. Such divergence could involve either a temporal separation in mating episodes, with small parasites maturing early, or a spatial separation, with small males being sexually-selected to mate near the nest with small queens seeking adoption, instead of in mating aggregations.

We conclude that inquiline species strictly following Emery's rule could have evolved by the intraspecific route. If so, such species provide evidence for West-Eberhard's “alternative adaptation” hypothesis that between-species diversity frequently stems from diversity within species. They also represent likely cases of sympatric speciation. We suggest work on the parasites' phytogeny, genetics, behaviour and mating biology to test these conclusions further.