The evolution of social parasitism in Acromyrmex leaf-cutting ants: a test of Emery?s rule

Abstract

Summary. Emery's rule predicts that social parasites and their hosts share common ancestry and are therefore likely to be close relatives. Within the leaf-cutting ant genus Acromyrmex, two taxa of social parasites have been found, which are thought to occupy opposite grades of permanent social parasitism, based on their contrasting morphologies: Acromyrmex insinuator differs little in morphology from its freeliving congeneric host species and produces a worker caste, and is thus thought to represent an early grade of social parasitism. At the other extreme, Pseudoatta spp. exhibit a very specialised morphology and lack a worker caste, both of which are characteristics of an evolutionarily derived grade of social parasitism. Here we present a molecular phylogeny using partial sequences of cytochrome oxidase I and II of about half of the known Acromyrmex species including two social parasites, their hosts and all congeneric species occurring sympatrically. We show that the two inquiline parasites represent two separate origins of social parasitism in the genus Acromyrmex. The early-grade social parasite A. insinuator is highly likely to be the sister species of its host Acromyrmex echinator, but the derived social parasite Pseudoatta sp. is not the sister species of its extant host Acromyrmex rugosus.

Origins of social parasitism: The importance of divergence ages in phylogenetic studies

“…The host-parasite relationships observed for Inquilina, B. falcata and Nasutapis all conform to either the strict or loose form of Emery's rule, and as such, are compatible with previous studies that have suggested social parasites evolved via sympatric speciation (Savolainen and Vepsäläi-nen, 2003;Sumner et al, 2004). However, the host-parasite relationships observed for the Macrogaiea social parasites are not consistent with an intra-specific origin via sympatric speciation.…”

“…The recent research on the phylogenetic relationships of social parasites with their hosts has produced many different results, some seeming to show strong support for sympatric speciation (Savolainen and Vepsäläinen, 2003;Sumner et al, 2004), while others appear to provide evidence against a sympatric origin of social parasites (Carpenter et al, 1993;Choudhary et al, 1994;Ward, 1996;Steiner et al, 2006). It may very well be that the different relationships obtained are due to the different divergence dates of the parasitic species used in each of these studies.…”

“…Emery's rule can be divided into two forms: the strict form, that states parasites are the closest relatives of their hosts, and the loose form, that states a parasite, or a group of parasites, are only closely related to their hosts. Recent molecular phylogenetic studies have revealed a mixture of these two forms in various ant and wasp groups (Savolainen and Vepsäläi-nen, 2003;Sumner et al, 2004) and the existence of sisterspecies relationships between hosts and parasites has been used to infer sympatric speciation (Buschinger, 1990;Bourke and Franks, 1991). At the same time, it is recognised that such inferential approaches can be problematic and further empirical evidence is required to more firmly distinguish between allopatric and sympatric hypotheses (Berlocher, 2003;Coyne and Orr, 2004).…”

“…Furthermore, these confounding factors would become increasingly more likely over time (Hey, 1992;Nee et al, 1994;Barraclough et al, 1998), so that phylogenetic approaches to the origin of social parasitism would be most effective when based on evolutionarily very recent origins (Parker and Rissing, 2002;Sumner et al, 2003;Sumner et al, 2004). The majority of molecular phylogenetic studies on the relationships of insect social parasites to their hosts have been based on ants, with fewer studies on wasps, and corbiculate and halictine bees.…”

Genetic Diversity and Disease Resistance in Leaf-Cutting Ant Societies

“…The individuals used came from the two most abundant patrilines in each colony, with the representation of these patrilines being matched for treatment. Panamanian Acromyrmex octospinosus and A. echinatior are closely related species (Sumner et al 2004b), and workers of A. octospinosus were used for the congeneric treatment. Ants were taken from three laboratory colonies (AoGP, AoAH, and Ao35) that had been collected at the same site in Gamboa, Panama, as that from which the A. echinatior colonies and the M. anisopliae var.…”