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Systematics and Population Genetics of Fire Ants (Solenopsis Saevissima Complex) from Argentina

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Systematics and Population Genetics of Fire Ants (Solenopsis Saevissima Complex) from Argentina Evolution, 44(8), 1990, pp, 2113-2134 SYSTEMATICS AND POPULATION GENETICS OF FIRE ANTS (SOLENOPSIS SAEVISSIMA COMPLEX) FROM ARGENTINA KENNETH G. Ross' AND JAMES C. TRAGER2 'Department ofEntomology, University ofGeorgia, Athens, GA 30602 USA -Depanmeni ofBiology, University ofMissouri-St. Louis, St. Louis, MO 63121 USA Abstract. - Specimens ofseven 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 ofreproductively isolated populations and partitioning ofintra- and interspecific vari­ ation can in most cases be achieved using appropriate characters ofeithertype in this taxonomically difficult group. Genetic differentiation between native (Argentina) and introduced(USA) conspecific populations oftwo species, Solenopsis invicta and S. richteri, is rather typical ofthe 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 ofthe 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 UnitedStates, suggesting that prezygotic barriers to gene flow have been compromised in introduced populations. Phylogenetic analysis ofthe 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 offitness, genomic incompatibilities generally may be insufficient to create effective postzygotic barriers to interspecific gene flow in this group ofants. Received August 29, 1989. Accepted April 18, 1990. The ants (family Formicidae) represent a 1989). Resolution of the taxonomic diffi­ remarkably successful lineage of ecologi­ culties created by such patterns of clado­ cally diverse, highly eusocial species, the genesis may in many instances require the systematics of which has suffered relative use of new character sets (e.g., molecular neglect given the ecological and economic markers) to define genetically isolatedgroups importance ofthe group. This neglect stems and to assess the distribution ofgenetic and in large part from considerable taxonomic morphological variability within and be­ difficulties at the species level. For instance, tween species. Because ant species com­ intraspecific geographic variability often prising taxonomically difficult groups are transcends interspecific variability in ants likely to be evolutionarily young, compar­ (e.g., Ward, 1984, 1989), leading to diffi­ ative population genetic and systematic culties in deciding the taxonomic status of studies of such groups may be particularly closely related populations when traditional informative with respect to the processes characters are studied in a limited number leading to reproductive isolation. of specimens. Furthermore, morphologi­ One group of ants in which the species­ cally cryptic species, that is, reproductively level taxonomy has posed continuing prob­ isolated populations in which morphologi­ lems is the Solenopsis saevissima species cal divergence is not evident, are sufficiently complex (subfamily Myrmicinae), mem­ common that most routine electrophoretic bers of which are commonly known as fire surveys have revealed previously unde­ ants. This complex, which includes rela­ scribed species (Crozier, 1977a, 1981; Ward, tively large-bodied forms with well devel­ 1980; Halliday, 1981; Crozier et al., 1986; oped worker polymorphism, is distributed Heinze, 1989; see also Ross et al., 1987a). naturally over a large part of the South These findings have been taken to suggest American continent east ofthe Andes. The that many groups of ants are in phases of taxonomy ofthe group has a history ofcon­ active radiation and that the process ofspe­ fusion and disagreement, with the number ciation may often be decoupled from sig­ offormally recognized taxa (species or sub­ nificant morphological evolution in these species) ranging from two to 17 (Buren, insects (see Crozier, 1977b; also Larson, 1972). A recent resurgence ofinterest in the 2113 2114 K. G. ROSS AND J. C. TRAGER FIG. 1. Distribution ofintroduced fire ants (Solenopsis saevissima complex) in the United States (modified from Diffieet al., 1988). Dotted line indicates approximate northernandwestern limits ofexpansion ofintroduced populations. Locations of three study populations of Ross et al. (1987a) resampled for this study are also indicated (Mor, Tur, Ala). systematics of these ants has come about (in an order characterized by male haploi­ for several reasons. First, fire ants intro­ dy), and loss of premating isolating mech­ duced to the United States have emerged as anisms associated with interspecific hybrid­ significant pests (Lofgren et aI., 1975). Sec­ ization (Brian, 1983 p. 259; Tschinkel and ond, the introduced species provide one of Nierenberg, 1983; Ross and Fletcher, 1985a; the few well-documented examples of an Ross et aI., 1987b). animal hybrid zone forming in historical Fire ants of the S. saevissima complex times (Vander Meer et aI., 1985; Ross et aI., were introduced to southern Alabama, in 1987b). Third, fire ants have become im­ the early part ofthis century and have since portant model systems for studying the evo­ become widespread throughout the south­ lution of social organization, the origin of eastern and south-central parts ofthe Unit­ reproductive isolation, and the relationship ed States (Fig. 1). Introduced populations, between these two facets ofevolution in ad­ originally assigned to the single variable vanced eusocial Hymenoptera (e.g., Wilson species Solenopsis saevissima (Creighton, and Brown, 1958; Crozier, 1979; Ross et 1930; Ettershank, 1966), have been consid­ aI., 1987a, 1988; Ward, 1989). Continued ered since the revision of Buren (1972) to progress ofresearch on all fronts will depend comprise two species, S. invicta and S. rich­ on an improved understanding ofthe taxo­ teri. The work ofBuren (Buren, 1972; Buren nomic status and phylogenetic affinities of et aI., 1974), based on morphological anal­ introduced and native fire ant populations, yses of specimens from the United States as can be obtained through an integrated and central South America, suggested that systematics/population genetics approach. S. invicta and S. richteri are phenotypically Furthermore, comparative population ge­ distinctive and internally quite uniform. netic data can shed light on the extent to Buren (1972) further concluded that hy­ which population bottlenecks have influ­ bridization between the two species is rare enced genetic structure in introduced pop­ or absent, despite the abundant opportunity ulations, an important consideration given for gene exchange between introduced pop­ that founder effects have been invoked to ulations in the United States. explain the origin ofsuch intriguing features A recent challenge to Buren's view has ofintroduced fire ants as polygyny (multiple come from the data of Vander Meer et aI. queens per colony), frequent male diploidy (1985). These authors, using gas chromato- FIRE ANT SYSTEMATICS AND POPULATION GENETICS 2115 graphic analyses of diagnostic micromo1e­ in the United States; 5) to obtain evidence cu1ar characters (hydrocarbons and venom bearing on the possibility of gene flow be­ alkaloids), provided evidence that hybrid­ tween fire ant species in their native ranges, ization commonly occurs between S. invicta particularly with reference to S. invicta and and S. richteri in east-central Mississippi. S. richteri; and 6) to infer phylogenetic re­ This has since been confirmed using elec­ lationships among the species. A related trophoretic markers (Ross et al., 1987b), and study in which morphological characters the zone ofhybridization between these in­ provide the basis ofa formal revision ofthe troduced forms is now known to encompass S. saevissima complex and allied taxa is pre­ a large area extending from eastern Missis­ sented elsewhere (Trager, 1990). sippi to northwestern Georgia (Diffie et al., 1988; see Fig. 1). Genetic analyses of the MATERIALS AND METHODS zone at its eastern and western extremes have revealed that genotype distributions at Sample Collections informative loci do not depart substantially Samples were collected from 201 nests of from distributions expected under Hardy­ Solenopsis distributed over 48 sites in Weinberg equilibrium and that a diverse ar­ northern Argentina (Buenos Aires, Santa Fe, ray ofrecombinant multilocus genotypes is Corrientes, Chaco, Formosa, Santiago del present (Ross et al., 1987b; Ross and Rob­ Estero, and Cordoba Provinces; see Fig. 2). ertson, 1990). These findings are consistent Wherever possible a series of nests (up to with panmixia in introgressed populations eight) ofthe same species was sampled at a and suggest that there is no large-scale single site (preliminary morphological iden­ breakdown in hybrid viability or fertility. tification was made in the field). Several These results from hybrid populations of winged female sexuals and workers were introduced S. invicta and S. richteri again taken from each nest, the former for elec­
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