Maternal effect killing by a supergene controlling ant social organization.

Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.

Unexpected patterns of segregation distortion at a selfish supergene in the fire ant Solenopsis invicta.

BACKGROUND: The Sb supergene in the fire ant Solenopsis invicta determines the form of colony social organization, with colonies whose inhabitants bear the element containing multiple reproductive queens and colonies lacking it containing only a single queen. Several features of this supergene - including suppressed recombination, presence of deleterious mutations, association with a large centromere, and "green-beard" behavior - suggest that it may be a selfish genetic element that engages in transmission ratio distortion (TRD), defined as significant departures in progeny allele frequencies from Mendelian inheritance ratios. We tested this possibility by surveying segregation ratios in embryo progenies of 101 queens of the "polygyne" social form (3512 embryos) using three supergene-linked markers and twelve markers outside the supergene. RESULTS: Significant departures from Mendelian ratios were observed at the supergene loci in 3-5 times more progenies than expected in the absence of TRD and than found, on average, among non-supergene loci. Also, supergene loci displayed the greatest mean deviations from Mendelian ratios among all study loci, although these typically were modest. A surprising feature of the observed inter-progeny variation in TRD was that significant deviations involved not only excesses of supergene alleles but also similarly frequent excesses of the alternate alleles on the homologous chromosome. As expected given the common occurrence of such "drive reversal" in this system, alleles associated with the supergene gain no consistent transmission advantage over their alternate alleles at the population level. Finally, we observed low levels of recombination and incomplete gametic disequilibrium across the supergene, including between adjacent markers within a single inversion. CONCLUSIONS: Our data confirm the prediction that the Sb supergene is a selfish genetic element capable of biasing its own transmission during reproduction, yet counterselection for suppressor loci evidently has produced an evolutionary stalemate in TRD between the variant homologous haplotypes on the "social chromosome". Evidence implicates prezygotic segregation distortion as responsible for the TRD we document, with "true" meiotic drive the most likely mechanism. Low levels of recombination and incomplete gametic disequilibrium across the supergene suggest that selection does not preserve a single uniform supergene haplotype responsible for inducing polygyny.

Foster carers influence brood pathogen resistance in ants.

Social organisms face a high risk of epidemics, and respond to this threat by combining efficient individual and collective defences against pathogens. An intriguing and little studied feature of social animals is that individual pathogen resistance may depend not only on genetic or maternal factors, but also on the social environment during development. Here, we used a cross-fostering experiment to investigate whether the pathogen resistance of individual ant workers was shaped by their own colony of origin or by the colony of origin of their carers. The origin of care-giving workers significantly influenced the ability of newly eclosed cross-fostered Formica selysi workers to resist the fungal entomopathogen Beauveria bassiana. In particular, carers that were more resistant to the fungal entomopathogen reared more resistant workers. This effect occurred in the absence of post-infection social interactions, such as trophallaxis and allogrooming. The colony of origin of eggs significantly influenced the survival of the resulting individuals in both control and pathogen treatments. There was no significant effect of the social organization (i.e. whether colonies contain a single or multiple queens) of the colony of origin of either carers or eggs. Our experiment reveals that social interactions during development play a central role in moulding the resistance of emerging workers.

Biodiversity assessment in incomplete inventories: leaf litter ant communities in several types of Bornean rain forest.

Biodiversity assessment of tropical taxa is hampered by their tremendous richness, which leads to large numbers of singletons and incomplete inventories in survey studies. Species estimators can be used for assessment of alpha diversity, but calculation of beta diversity is hampered by pseudo-turnover of species in undersampled plots. To assess the impact of unseen species, we investigated different methods, including an unbiased estimator of Shannon beta diversity that was compared to biased calculations. We studied alpha and beta diversity of a diverse ground ant assemblage from the Southeast Asian island of Borneo in different types of tropical forest: diperocarp forest, alluvial forest, limestone forest and heath forests. Forests varied in plant composition, geology, flooding regimes and other environmental parameters. We tested whether forest types differed in species composition and if species turnover was a function of the distance between plots at different spatial scales. As pseudo-turnover may bias beta diversity we hypothesized a large effect of unseen species reducing beta diversity. We sampled 206 ant species (25% singletons) from ten subfamilies and 55 genera. Diversity partitioning among the four forest types revealed that whereas alpha species richness and alpha Shannon diversity were significantly smaller than expected, beta-diversity for both measurements was significantly higher than expected by chance. This result was confirmed when we used the unbiased estimation of Shannon diversity: while alpha diversity was much higher, beta diversity differed only slightly from biased calculations. Beta diversity as measured with the Chao-Sørensen or Morisita-Horn Index correlated with distance between transects and between sample points, indicating a distance decay of similarity between communities. We conclude that habitat heterogeneity has a high influence on ant diversity and species turnover in tropical sites and that unseen species may have only little impact on calculation of Shannon beta diversity when sampling effort has been high.

Division of labor in the hyperdiverse ant genus Pheidole is associated with distinct subcaste- and age-related patterns of worker brain organization.

The evolutionary success of ants and other social insects is considered to be intrinsically linked to division of labor among workers. The role of the brains of individual ants in generating division of labor, however, is poorly understood, as is the degree to which interspecific variation in worker social phenotypes is underscored by functional neurobiological differentiation. Here we demonstrate that dimorphic minor and major workers of different ages from three ecotypical species of the hyperdiverse ant genus Pheidole have distinct patterns of neuropil size variation. Brain subregions involved in sensory input (optic and antennal lobes), sensory integration, learning and memory (mushroom bodies), and motor functions (central body and subesophageal ganglion) vary significantly in relative size, reflecting differential investment in neuropils that likely regulate subcaste- and age-correlated task performance. Worker groups differ in brain size and display patterns of altered isometric and allometric subregion scaling that affect brain architecture independently of brain size variation. In particular, mushroom body size was positively correlated with task plasticity in the context of both age- and subcaste-related polyethism, providing strong, novel support that greater investment in this neuropil increases behavioral flexibility. Our findings reveal striking levels of developmental plasticity and evolutionary flexibility in Pheidole worker neuroanatomy, supporting the hypothesis that mosaic alterations of brain composition contribute to adaptive colony structure and interspecific variation in social organization.

Potential cause of lethality of an allele implicated in social evolution in fire ants.

The gene Gp-9 is believed to have a major effect on colony social organization in fire ants, with the presence of b-like alleles in a colony associated with multiple-queen (polygyne) organization. Queens and workers of polygyne Solenopsis invicta homozygous for the b-like allele designated b suffer reduced viability compared to other genotypes, and bb queens do not survive to become egg-layers. Thus, the b allele effectively acts as a recessive lethal. This allele differs from the remaining b-like alleles (designated b'), as well as all other Gp-9 alleles, by encoding a lysine at position 151 in the protein product, suggesting that this substitution is responsible for its deleterious effects. We tested this hypothesis by comparing frequencies of b'b' and bb homozygotes, first in queens of Solenopsis richteri and S. invicta, then in S. invicta workers from populations polymorphic for the two b-like alleles. We found that almost 20% of S. richteri queens were b'b' homozygotes, compared to the virtual absence of bb homozygotes among S. invicta queens, and that 5-18% of S. invicta workers bore genotype b'b', compared to the apparent lack of bb workers in the same populations. While we cannot entirely rule out involvement of other genes in complete gametic disequilibrium with Gp-9, our data are consistent with the hypothesis that the Lys(151) residue in GP-9 protein confers the deleterious effects of the b allele in homozygous condition, possibly by impairing the protein's function through interference with ligand binding/release or hindrance of dimer formation.

Genetic caste determination in Pogonomyrmex harvester ants imposes costs during colony founding.

Some populations of Pogonomyrmex harvester ants comprise genetically differentiated pairs of interbreeding lineages. Queens mate with males of their own and of the alternate lineage and produce pure-lineage offspring which develop into queens and inter-lineage offspring which develop into workers. Here we tested whether such genetic caste determination is associated with costs in terms of the ability to optimally allocate resources to the production of queens and workers. During the stage of colony founding, when only workers are produced, queens laid a high proportion of pure-lineage eggs but the large majority of these eggs failed to develop. As a consequence, the number of offspring produced by incipient colonies decreased linearly with the proportion of pure-lineage eggs laid by queens. Moreover, queens of the lineage most commonly represented in a given mating flight produced more pure-lineage eggs, in line with the view that they mate randomly with the two types of males and indiscriminately use their sperm. Altogether these results predict frequency-dependent selection on pairs of lineages because queens of the more common lineage will produce more pure-lineage eggs and their colonies be less successful during the stage of colony founding, which may be an important force maintaining the coexistence of pairs of lineages within populations.

Alternative genetic foundations for a key social polymorphism in fire ants.

Little is known about the genetic foundations of colony social organization. One rare example in which a single major gene is implicated in the expression of alternative social organizations involves the presumed odorant-binding protein gene Gp-9 in fire ants. Specific amino acid substitutions in this gene invariably are associated with the expression of monogyny (single queen per colony) or polygyny (multiple queens per colony) in fire ant species of the Solenopsis richteri clade. These substitutions are hypothesized to alter the abilities of workers to recognize queens and thereby regulate their numbers in a colony. We examined whether these same substitutions underlie the monogyny/polygyny social polymorphism in the distantly related fire ant S. geminata. We found that Gp-9 coding region sequences are identical in the polygyne and monogyne forms of this species, disproving our hypothesis that one or a few specific amino acid replacements in the protein are necessary to induce transitions in social organization in fire ants. On the other hand, polygyne S. geminata differs genetically from the monogyne form in ways not mirrored in the two forms of S. invicta, a well-studied member of the S. richteri clade, supporting the conclusion that polygyny did not evolve via analogous routes in the two lineages. Specifically, polygyne S. geminata has lower genetic diversity and different gene frequencies than the monogyne form, suggesting that the polygyne form originated via a founder event from a local monogyne population. These comparative data suggest an alternative route to polygyny in S. geminata in which loss of allelic variation at genes encoding recognition cues has led to a breakdown in discrimination abilities and the consequent acceptance of multiple queens in colonies.