Populations composed entirely of hybrid colonies: bidirectional hybridization and polyandry in harvester ants KIRK E. ANDERSON*, STEPHEN J. NOVAK and JAMES F. SMITH Department of Biology, Boise State University, 1910 University Drive, Boise, ID 83725, USA Received 21 January 2008; accepted for publication 9 January 2008 In eusocial Hymenoptera, haplodiploid life cycles, obligate sterile castes, and polyandry may facilitate selection for hybridization. We analyzed a broad hybrid zone between the ecologically distinct seed-harvester ants Pogono- myrmex occidentalis (Cresson) and Pogonomyrmex maricopa (Wheeler) using mitochondrial (mt)DNA sequence data, eight morphological markers, and 14 random amplified polymorphic DNA (RAPD) markers. Average mtDNA sequence divergence among parental species was 11.34%, indicating secondary contact. RAPD markers were significantly correlated with morphological variation, confirming the interspecific hybrid origin of all morphologi- cally putative hybrid colonies. A morphological hybrid index indicates an abundance of both F1 hybrids and parental morphotypes within colonies. Individual character frequencies plotted against distance show coincident and concordant clines, suggesting little to no introgression. The structure of the hybrid zone is two-fold. Within the western region, stark reversals in character frequencies coincide with overt soil differences, indicating a mosaic hybrid zone structure. The eastern region is a riparian habitat where four adjacent populations were composed entirely of hybrid colonies. These habitat associations suggest that hybrid worker genomes permit dispersal into intermediate environments that select against one or both parental species. The present study suggests that, in addition to retaining reproductive compatibility, ecologically distinct species of ants may generate hybrid colonies maintained by environmental selection. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 320–336. ADDITIONAL KEYWORDS: colony level selection – dependent lineages – exogenous selection – genetic caste determination – heterosis – hybrid fitness – maricopa – mosaic hybrid zone – occidentalis – Pogonomyrmex. INTRODUCTION Although plant hybridization is known to be adaptive (Lewontin & Birch, 1966; Burke, Carney & Arnold, 1998) and may commonly generate new species (Riese- berg, 1997), animal hybridization is generally con- sidered an unfortunate consequence of incomplete speciation (Arnold, 1997); but see also (Grant & Grant, 1996). The interbreeding of differentially adapted species is expected to result in genomic incompatibil- ities and reduced hybrid fitness (Dobzhansky, 1940; Muller, 1942; Mayr, 1963). In general, this selection pressure is expected to increase with genetic diver- gence (i.e. selection is less between races or recently diverged sibling species; Bermingham et al., 1992; Coyne & Orr, 1997; Lovette & Bermingham, 1999). Cases have been described, however, wherein species pairs with little genetic differentiation show reduced hybrid fitness or sterility, whereas pairs with high differentiation can interbreed freely producing a hybrid swarm with no detectable fitness loss (Jiggins & Mallet, 2000). A number of studies have also revealed that F 1 hybrid fitness can exceed that of either parent in certain habitats (Moore, 1977; Emms & Arnold, 1997; Burke et al., 1998; Burke & Arnold, 2001). The spatial structure of a hybrid zone is an indica- tion of processes that maintain hybridization (Endler, *Corresponding author. Current address: Department of Entomology, Center for Insect Science, PO Box 210036, University of Arizona, Tucson, AZ 85721, USA. E-mail: keanders@email.arizona.edu Biological Journal of the Linnean Society, 2008, 95, 320–336. With 5 figures © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95, 320–336 320 Downloaded from https://academic.oup.com/biolinnean/article-abstract/95/2/320/2701287 by guest on 20 May 2020