Kenneth G. Ross

Selfish genes: a green beard in the red fire ant

A ‘green-beard’ gene is defined as a gene that causes a phenotypic effect (such as the presence of a green beard or any other conspicuous feature), allows the bearer of this feature to recognize it in other individuals, and causes the bearer to behave differently towards other individuals depending on whether or not they possess the feature. Such genes have been proposed on theoretical grounds to be agents mediating both altruism and intragenomic conflicts,, but until now few, if any, of these genes have been identified,. Here we provide evidence of a green-beard gene in the red imported fire ant, Solenopsis invicta. In polygyne (multiple-queen) colonies, all egg-laying queens are Bb heterozygotes at the locus Gp-9 (ref. 6). Previous studies suggested that bb females die prematurely from intrinsic causes; we now show that BB queens initiating reproduction are killed by workers, and that it is primarily Bb rather than BB workers that are responsible for these executions. This implies that allele Gp-9b is linked to a green-beard allele that preferentially induces workers bearing the allele to kill all queens that do not bear it. Workers appear to distinguish BB from Bb queens on the basis of a transferable odour cue.

Molecular ecology of social behaviour: analyses of breeding systems and genetic structure

Molecular genetic studies of group kin composition and local genetic structure in social organisms are becoming increasingly common. A conceptual and mathematical framework that links attributes of the breeding system to group composition and genetic structure is presented here, and recent empirical studies are reviewed in the context of this framework. Breeding system properties, including the number of breeders in a social group, their genetic relatedness, and skew in their parentage, determine group composition and the distribution of genetic variation within and between social units. This group genetic structure in turn influences the opportunities for conflict and cooperation to evolve within groups and for selection to occur among groups or clusters of groups. Thus, molecular studies of social groups provide the starting point for analyses of the selective forces involved in social evolution, as well as for analyses of other fundamental evolutionary problems related to sex allocation, reproductive skew, life history evolution, and the nature of selection in hierarchically structured populations. The framework presented here provides a standard system for interpreting and integrating genetic and natural history data from social organisms for application to a broad range of evolutionary questions.

Global Invasion History of the Fire Ant Solenopsis invicta

Argentine fire ants have spread around the world from a population that was first established a century ago in North America. 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.

Comparative study of genetic and social structure in two forms of the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

SummaryThe genetic and social structures of polygyne and monogyne forms of the fire ant, Solenopsis invicta, are investigated in a comparative manner using allozyme data from two polymorphic loci. Foundress queens of the monogyne form are signly inseminated and appear to produce all males present in the colony during the major summer mating flights. The average regression coefficient of relatedness (b) among female nestmates of the monogyne form is 0.714 (Fig. 2), statistically indistinguishable from the pedigree coefficient of relatedness (G) of 0.75. We suggest that the evolution of obligate worker sterility in Solenopsis is associated with this high relatedness between workers and the queens they rear. Functional queens in polygyne nests also are singly inseminated and are no more closely related to nestmate queens than to other queens (within-nest b=0). Within-nest relatedness of workers in the polygyne population is similarly low (Fig. 2). Both the monogyne and polygyne populations from northcentral Georgia are in Hardy-Weinberg equilibrium at both allozyme loci and we found no evidence of significant population subdividion or inbreeding in the polygyne population. These results do not support the view that kin selection has promoted the evolution of polygyny in North American S. invicta. Rather, mutualism appears to be the most likely selective factor mediating queen associations inthis ant.

Genetic origin of male diploidy in the fire ant, Solenopsis invicta (Hymenoptera : Formicidae), and its evolutionary significance

Male diploidy was studied in natural populations of the fire ant, Solenopsis invicta, in order to find an explanation from population genetics for the apparently common occurrence of this phenomenon in some North American populations. The association of male diploidy with polygyne (more than one queen per colony) populations in this species led us to expect that the two phenomena are causally linked. We proposed three hypotheses, based on current knowledge of sex‐determining mechanisms in the Hymenoptera, to explain the loss of genetic diversity associated with high rates of diploid male production in S. invicta: a) allelic diversity was reduced during colonization of North America by a small founder group; b) allelic diversity was reduced during subsequent subfounding of the several polygyne populations; and c) genetic structuring of polygyne populations due to local inbreeding caused reduced allelic diversity and/or increased homozygosity.

The Breeding System of the Fire Ant Solenopsis invicta: Effects on Colony Genetic Structure

Genetic and observational data are combined to describe the breeding system in a polygyne population of Solenopsis invicta using a formal theoretical framework that links properties of the breeding system with colony genetic structure. Queens of S. invicta mate only once, and the study population is outbred. The number of mated queens per nest is variable but generally low, with the average relatedness of nest-mate queens indistinguishable from zero. The genetic data are sufficiently complete that worker relatedness in individual nests can be estimated accurately, and the values obtained are shown to be well accounted for by the number of queens present in each nest. Thus, variance in maternity apportionment among nest-mate queens or internest movement of ants need not be invoked as determinants of colony genetic structure. Average worker nest-mate relatedness results from the opposing effects of two groups of factors: single mating by queens and the apparent closed nature of the societies elevate relatedness, while the presence of multiple queens and their low relatedness to one another depress it. This study also reveals consistent differences within nests in the matrilineal composition of worker and queen brood. This constitutes further evidence for inequities among nest-mate queens in the allocation of their progeny to the two castes at a single point in time.

Diploid male production — a significant colony mortality factor in the fire ant Solenopsis invicta (Hymenoptera: Formicidae)

SummaryTwo forms of the fire ant, Solenopsis invicta, occur in North America; the monogyne form has colonies with a single functional queen while the polygyne form has colonies containing many functional queens. Field surveys indicate that diploid males are common in natural populations of the polygyne form but absent from monogyne populations, in contrast to laboratory data showing that similar frequencies of queens producing such males occur in the two types of populations. Our results show that mature monogyne colonies with adopted queens rear diploid males in the laboratory, so it is unlikely that the absence of these males from monogyne colonies in the field is due to discrimination against them by monogyne workers. On the other hand, incipient monogyne colonies that produce diploid males exhibit significantly higher mortality and significantly slower rates of growth (Figs. 1–3) than colonies producing workers only. These results suggest that the observed distribution of male diploidy in S. invicta can be explained by differential mortality of diploid male producing colonies of the two forms, with such colonies of the monogyne form experiencing 100% mortality early in development. The mortality differences due to this factor are shown to be related to the different social structures and modes of colony founding characterizing the two forms.

BIOCHEMICAL PHENOTYPIC AND GENETIC STUDIES OF TWO INTRODUCED FIRE ANTS AND THEIR HYBRID (HYMENOPTERA: FORMICIDAE)

Two introduced fire ants, Solenopsis invicta and S. richteri, and their hybrid were studied using phenotypic markers from gas chromatographic analysis of hydrocarbons and venom alkaloids, as well as genetic markers from enzyme electrophoresis. Both methods show that extensive gene introgression is occurring over a distance of at least 120 km at the contact zone between the two forms in eastern Mississippi. Genetic analyses suggest that the hybrid population does not depart dramatically from panmixia. Also, recombinant genotypes predominate in the hybrid zone, indicating that F1 hybrids are viable. Allele frequency clines through the hybrid zone are apparent for four polymorphic loci. Data sets generated by the chromatographic and electrophoretic methods are highly concordant in that they differentiate completely between the two forms and agree in designating colonies from the contact zone as hybrid or parental in a high proportion (90%) of cases. The two methods can serve as complementary tools for studying closely related but genetically distinct populations in this, and perhaps other, groups of insects.

The Natural Selection of Sexual Cannibalism

Sexual cannibalism, in which a male is eaten by his mate following copulation, is expected to convey a selective advantage to the male under certain conditions. As shown quantitatively in our model the phenomenon is expected when (1) a male can mate only a few times in his lifetime and (2) the cannibalism significantly increases the number and/or viability of eggs fertilized by his own sperm. The expected number of male matings appears to be the more important of these two conditions. The few available observations of sexual cannibalism in several species of arthropods agree qualitatively with the predictions of our model. The same parameters of the model also explain why sexual cannibalism is generally rare among vertebrates. Phenomena selecting for sexual cannibalism appear more closely related to paternal investment strategies than to ecological factors associated with other forms of cannibalism. Because few field studies of invertebrates have followed the mating history of marked males, we cannot test our model quantitatively with existing data. We suggest specific field observations which would provide quantitative estimates of the expected number of male matings. In addition we describe possible laboratory experiments which would give more precise measurements of the increase in fecundity of the cannibalized male.

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.