Pekka Pamilo

The genome of the fire ant Solenopsis invicta

Ants have evolved very complex societies and are key ecosystem members. Some ants, such as the fire ant Solenopsis invicta, are also major pests. Here, we present a draft genome of S. invicta, assembled from Roche 454 and Illumina sequencing reads obtained from a focal haploid male and his brothers. We used comparative genomic methods to obtain insight into the unique features of the S. invicta genome. For example, we found that this genome harbors four adjacent copies of vitellogenin. A phylogenetic analysis revealed that an ancestral vitellogenin gene first underwent a duplication that was followed by possibly independent duplications of each of the daughter vitellogenins. The vitellogenin genes have undergone subfunctionalization with queen- and worker-specific expression, possibly reflecting differential selection acting on the queen and worker castes. Additionally, we identified more than 400 putative olfactory receptors of which at least 297 are intact. This represents the largest repertoire reported so far in insects. S. invicta also harbors an expansion of a specific family of lipid-processing genes, two putative orthologs to the transformer/feminizer sex differentiation gene, a functional DNA methylation system, and a single putative telomerase ortholog. EST data indicate that this S. invicta telomerase ortholog has at least four spliceforms that differ in their use of two sets of mutually exclusive exons. Some of these and other unique aspects of the fire ant genome are likely linked to the complex social behavior of this species.

Polyandry and allele frequency differences between the sexes in the ant Formica aquilonia

Genetic mother-offspring analyses based on six enzyme gene loci show that about 60 per cent of the females of the mound-building red wood ant Formica aquilonia mate with several males. The number of matings inferred from the offspring genotypes range from one to six, the arithmetic mean being 1.94. The mates do not contribute equally in the inseminations; in the case of two matings, one male is estimated to inseminate on average 77 per cent of the offspring. The average related-ness among the offspring of a single female is 0.6, corresponding to the effective number of matings of 1.43. Three of the six loci show remarkable allele frequency differences between the sexes. At each of these loci the males virtually lack the alleles present in females with frequencies 0.18 at Me, 0.25 at Pgk and 0.27 at Gpi. Segregation analyses indicate normal Mendelian inheritance at these loci and the difference between the sexes seem likely to result from selection.

Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites

Complex eusocial insect societies are generally matrifilial, suggesting kin selection has been of importance in their development. For simpler social systems, factors favouring their existence, in particular kin selection, have rarely been studied. Communal nesting is one of these simple social organizations, and is found in a diversity of insect species. To examine whether kin selection may play a role in the evolution and maintenance of communality, we estimated genetic relatedness of nestmate females of the facultatively communal bee, Andrena jacobi. Microsatellite loci were developed for this species and used to analyse individuals from two populations. Loci were variable, they were in heterozygote deficit and showed positive inbreeding coefficients. This may arise from nonrandom mating; previous observations (Paxton & Tengö 1996) indicate that a large proportion of females mate intranidally with nestmate males in their natal nests before first emerging. Nestmate relatedness was low, no different from zero for all loci in one population and for three of four loci in the other population. The large number of nestmates sharing a common nest (up to 594) may explain the low relatedness estimates, although relatedness was also independent of the number of females sharing a nest. Lack of inclusive fitness payoffs could constrain social evolution in this communal species.

Accumulation of mutations in sexual and asexual populations

The accumulation of beneficial and harmful mutations in a genome is studied by using analytical methods as well as computer simulation for different modes of reproduction. The modes of reproduction examined are biparental (bisexual, hermaphroditic), uniparental (selfing, automictic, asexual) and mixed (partial selfing, mixture of hermaphroditism and parthenogenesis). It is shown that the rates of accumulation of both beneficial and harmful mutations with weak selection depend on the within-population variance of the number of mutant genes per genome. Analytical formulae for this variance are derived for neutral mutant genes for hermaphroditic, selfing and asexual populations; the neutral variance is largest in a selfing population and smallest in an asexual population. Directional selection reduces the population variance in most cases, whereas recombination partially restores the reduced variance. Therefore, biparental organisms accumulate beneficial mutations at the highest rate and harmful mutations at the lowest rate. Selfing organisms are intermediate between biparental and asexual organisms. Even a limited amount of outcrossing in largely selfing and parthenogenetic organisms markedly affects the accumulation rates. The accumulation of mutations is likely to affect the mean population fitness only in long-term evolution.

GENE FLOW AND POPULATION VISCOSITY IN MYRMICA ANTS

The amount of gene flow and population viscosity were studied in two red ant species, Myrmica ruginodis and M. rubra. Differentiation between populations at the local scale (within the dispersal distance of individuals) and between localities further apart was estimated using Wrights F-statistics. Population viscosity was described using spatial autocorrelation of allele frequencies of nests. The differentiation patterns in the two species are clearly distinct, FST values being an order of magnitude larger in M. rubra (M. rubra: FST = 0.205 between sites within localities and 0.199 between localities; M. ruginodis: FST = 0.027 and 0.014 between sites within localities, 0.009 between localities). Thus, assuming the island model, much less gene flow occurs between neighbouring M. rubra than M. ruginodis sites. Allele frequencies of nests close to each other are positively autocorrelated in both species. This suggests that new nests are commonly founded close to the mother nest, most probably by division of existing nests. M. rubra forms large multinest societies, which dominate substantial areas, whereas such multinest colonies are rare in M. ruginodis.

Nestmate recognition and the genetic relatedness of nests in the ant Formica pratensis

Genetic relatedness of the mound-building ant Formica pratensis was determined by means of microsatellite DNA polymorphism, and its impact on nestmate recognition was tested in a population in Southern Sweden (Oeland). Recognition between nests was measured by testing aggression levels between single pairs of workers. The genetic distances of nests (Neis genetic distance) and the spatial distance of nests were correlated and both showed a strong relation to the aggression behavior. Multiple regression analysis revealed a stronger impact of genetic relatedness rather than spatial distances on aggression behavior. Neighbouring nests were more closely related than distant nests, which may reflect budding as a possible spreading mechanism. The genetic distance data showed that nestmate recognition was strongly genetically influenced in F. pratensis.

Diploid males and colony-level selection in Formica ants

It is suggested that the evolution of polyandry by social hymenopteran queens is caused by colony-level selection, either because polyandry affects the distribution of non-functional diploid males in colonies (the load hypothesis) or because it increases the genetic diversity of the worker force (the diversity hypothesis). Diploid males that arise from fertilized eggs thai are homozygous at the sex-determining locus (or loci) are inviable or infertile. Models of the load hypothesis analysed in this study suggest that slow growth and high mortality of colonies with diploid males favour single mating by queens. The longer the period ol colony growth (the period with selective differences) and the heavier the mortality, the stronger is the selection for monandry. The load hypothesis also predicts an association between monogyny and monandry. In contrast, the diversity hypothesis predicts an association between monogyny and polyandry, as multiple mating offers a way by which a monogynous colony could increase...

Genetic population structure in polygynous formica ants

SummaryGenetic population structures, both mating and interaction structures, were investigated in three polygynous Formica ants by examining how genotype frequencies are distributed among the nests in their populations. The study is based on electrophoretically analysed enzyme polymorphisms. The patterns of genotypic variation among single-nest workers suggest that polygyny is functional in all the three species. The observed genotype frequencies indicate outbreeding within the study areas, and no spatial microdifferentiation in gene frequencies is detected. The coexistent gynes in nests of both F. transkaucasica and F. polyctena are genetically related to each other, and the same holds for worker nest mates. These results support the hypothesis that polygyny is favoured by kin selection. The lack of genetic relatedness among gyne nest mates in the highly polygynous F. aquilonia suggests that additional factors, such as mutualism or parental parasitism, are probably involved in the evolution of polygyny.

Intranest relatedness and nestmate recognition in the meadow ant Formica pratensis (R.)

Abstract. The impact of intranest relatedness on nestmate recognition was tested in a population of polydomous and monodomous nests of the mound-building ant Formica pratensis. Nestmate recognition was evaluated by testing aggression levels between 37 pairs of nests (n=206 tests). Workers from donor colonies were placed on the mounds of recipient nests to score aggressive interactions among workers. A total of 555 workers from 27 nests were genotyped using four DNA microsatellites. The genetic and spatial distances of nests were positively correlated, indicating budding and/or fissioning as spread mechanisms. Monodomous and polydomous nests did not show different aggression levels. Aggression behavior between nests was positively correlated with both spatial distance and intranest relatedness of recipient colonies, but not with genetic distance or intranest relatedness of donor colonies. Multiple regression analysis revealed a stronger effect of spatial distance than of genetics on aggression behavior in this study, indicating that the relative importance of environment and genetics can be variable in F. pratensis. Nevertheless, the positive regression between intranest relatedness of recipient colonies and aggression in the multiple analysis supports earlier results that nestmate recognition is genetically influenced in F. pratensis and further indicates that foreign label rejection most likely explains our data.

Genetic structure of nests in the ant Formica sanguinea

Summary1.Polymorphism at an enzyme locus encoding for malate dehydrogenase was studied in 92 nests of the ant Formica sanguinea, mainly in Finland. Four alleles segregated at the locus. In seven nests all workers were homozygous for a single allele. In all other nests heterozygotes were observed. Of the nests, 75% were two-genotype nests having mainly one homozygous and one heterozygous worker genotype.2.Each single nest could be explained as the offspring of one gyne, but this interpretation does not agree with the expectations at the population level. The distribution of different nest types was compared with the results obtained by various computer-simulated reproductive strategies. The observations were best explained by several related, single-mated gynes per nest, and by one gyne possibly dominating the egg-laying. This agrees with earlier field observations and is also supported by the level of genetic relatedness among nestmates.3.In two successive years, the average coefficients of relatedness (b±SE) among workers of a single nest in one population were 0.420±0.098 and 0.311±0.124. As the coefficient of relatedness of the female brood to the workers of the same nest was 0.378±0.173, the brood that the workers care for is less closely related to them than their own offspring would be. The relatedness of the male brood to the workers was b=0.616±0.402. Worker ants of neighbouring nests were related to one another, b=0.248±0.093, presumably due to existence of sister nests.