The origin and sequential radiation of the social parasite Tamalia inquilinus (Hemiptera: Aphididae)

Tamalia is a genus of galling aphids found on plants in the family Ericaceae in western North America.  These aphids induce hollow galls, outgrowths composed of plant tissue serving as protective and nutritional microhabitat.  Tamalia inquilinus is  unique in its genus in that it cannot induce galls. This species must instead occupy the galls of other Tamalia aphids in order to survive and reproduce: this socially parasitic behavior is known as inquilinism.  The evolutionary origins of inquilinism are not completely understood.  An earlier analysis of Tamalia mitochondrial DNA suggested a single origin of inquilinism in the aphid lineage and that the social parasites evolved from their hosts in sympatry. In order to better describe the full evolutionary history of Tamalia aphids, we created multiple Bayesian phylogenies using data from the nuclear aphid genome and maternally-inherited Buchnera genome.  Our results confirmed a single origin of inquiline behavior from a gall-inducing host. The exact mechanism of divergence (whether through sympatry or allopatry), however, remains unclear.  Our data show greater topological structure within the inquiline clades, and surprisingly, greater divergence between populations on different host plants than their gall-forming hosts. One explanation for the pattern of synchronous divergence between gall-forming and inquiline aphids is that the social parasites are undergoing rapid and sequential radiation with their host aphids. These findings call into question previous assumptions about parasitism and the forces that cause diversity.