Global invasion history of the fire ant Solenopsis invicta.

The fire ant Solenopsis invicta is a significant pest that was inadvertently introduced into the southern United States almost a century ago and more recently into California and other regions of the world. An assessment of genetic variation at a diverse set of molecular markers in 2144 fire ant colonies from 75 geographic sites worldwide revealed that at least nine separate introductions of S. invicta have occurred into newly invaded areas and that the main southern U.S. population is probably the source of all but one of these introductions. The sole exception involves a putative serial invasion from the southern United States to California to Taiwan. These results illustrate in stark fashion a severe negative consequence of an increasingly massive and interconnected global trade and travel system.

Species delimitation: a case study in a problematic ant taxon.

Species delimitation has been invigorated as a discipline in systematics by an influx of new character sets, analytical methods, and conceptual advances. We use genetic data from 68 markers, combined with distributional, bioclimatic, and coloration information, to hypothesize boundaries of evolutionarily independent lineages (species) within the widespread and highly variable nominal fire ant species Solenopsis saevissima, a member of a species group containing invasive pests as well as species that are models for ecological and evolutionary research. Our integrated approach uses diverse methods of analysis to sequentially test whether populations meet specific operational criteria (contingent properties) for candidacy as morphologically cryptic species, including genetic clustering, monophyly, reproductive isolation, and occupation of distinctive niche space. We hypothesize that nominal S. saevissima comprises at least 4-6 previously unrecognized species, including several pairs whose parapatric distributions implicate the development of intrinsic premating or postmating barriers to gene flow. Our genetic data further suggest that regional genetic differentiation in S. saevissima has been influenced by hybridization with other nominal species occurring in sympatry or parapatry, including the quite distantly related Solenopsis geminata. The results of this study illustrate the importance of employing different classes of genetic data (coding and noncoding regions and nuclear and mitochondrial DNA [mtDNA] markers), different methods of genetic data analysis (tree-based and non-tree based methods), and different sources of data (genetic, morphological, and ecological data) to explicitly test various operational criteria for species boundaries in clades of recently diverged lineages, while warning against over reliance on any single data type (e.g., mtDNA sequence variation) when drawing inferences.

Phylogeographic structure of the fire ant Solenopsis invicta in its native South American range: roles of natural barriers and habitat connectivity.

We generated mitochondrial DNA (mtDNA) sequence data from 402 individuals of the fire ant Solenopsis invicta collected from 11 native populations and analyzed these data using a combination of demographic, phylogenetic, and phylogeographic methods to infer features of the evolutionary history of this species. Prior expectations regarding high levels of genetic structure and isolation by distance among populations were supported by the data, but we also discovered several unanticipated patterns. Our analyses revealed a major genetic break between S. invicta mtDNA haplotypes that coincides with the Mesopotamia wetlands region of South America, resulting in two higher level nested clade groupings. In addition, we identified contrasting patterns of genetic differentiation within these two major groups, which may reflect differences in connectivity of suitable habitat in different parts of the native range of S. invicta. Our study represents the first attempt to understand the phylogeographic history of S. invicta across its native range.

Species delimitation in native South American fire ants.

The taxonomy of fire ants has been plagued by difficulties in recognizing species on the basis of morphological characters. We surveyed allozyme markers and sequences of the mtDNA COI gene in several closely related nominal species from two areas of sympatry in the native ranges to learn whether the morphology-based delimitation of these species is supported by genetic data. We found that Solenopsis invicta and Solenopsis richteri, pest species whose distinctiveness has been debated, appear to be fully reproductively isolated at both study sites. This isolation contrasts with the extensive hybridization occurring between them in the USA, where both have been introduced. We also found strong genetic differentiation consistent with barriers to gene flow between Solenopsis quinquecuspis and the other two species. However, several lines of evidence suggest that nuclear and mitochondrial genes of S. invicta and S. richteri are introgressing into S. quinquecuspis. The latter apparently is a recently derived member of the clade that includes all three species, suggesting that there has been insufficient time for its full development of intrinsic isolating mechanisms. Finally, our discovery of genetically distinct populations within both S. invicta and S. richteri suggests the presence of previously unrecognized (cryptic) species. Their existence, together with the difficulties in developing diagnostic morphological characters for described species, imply that the group is actively radiating species and that morphological divergence generally does not keep pace with the development of reproductive isolation and neutral genetic divergence in this process.

Identification of a major gene regulating complex social behavior.

Colony queen number, a major feature of social organization in fire ants, is associated with worker genotypes at the gene Gp-9. We sequenced Gp-9 and found that it encodes a pheromone-binding protein, a crucial molecular component in chemical recognition of conspecifics. This suggests that differences in worker Gp-9 genotypes between social forms may cause differences in workers' abilities to recognize queens and regulate their numbers. Analyses of sequence evolution indicate that regulation of social organization by Gp-9 is conserved in South American fire ant species exhibiting social polymorphism and suggest that positive selection has driven the divergence between the alleles associated with alternate social organizations. This study demonstrates that single genes of major effect can underlie the expression of complex behaviors important in social evolution.

SYSTEMATICS AND POPULATION GENETICS OF FIRE ANTS (SOLENOPSIS SAEVISSIMA COMPLEX) FROM ARGENTINA.

Specimens of seven fire ant species collected from their native ranges in Argentina were studied by protein electrophoresis and morphological analysis. Concordance between the genetic and morphological character sets is strong (96% agreement on identifications), suggesting that recognition of reproductively isolated populations and partitioning of intra- and interspecific variation can in most cases be achieved using appropriate characters of either type in this taxonomically difficult group. Genetic differentiation between native (Argentina) and introduced (USA) conspecific populations of two species, Solenopsis invicta and S. richteri, is rather typical of the differentiation existing between conspecific populations found within either country. Furthermore, there appears to have been little reduction of variability (heterozygosity) at enzyme loci following colonization by either species of the United States, although some rare alleles have been lost in the introduced populations. Hybridization is rare between S. invicta and S. richteri where their native ranges overlap in central Argentina, in contrast to the extensive hybridization of these species in the United States, suggesting that prezygotic barriers to gene flow have been compromised in introduced populations. Phylogenetic analysis of the seven species indicates that S. invicta and S. richteri are relatively distantly related within the S. saevissima complex. Given that hybrids between these species in the United States suffer little apparent loss of fitness, genomic incompatibilities generally may be insufficient to create effective postzygotic barriers to interspecific gene flow in this group of ants.