Complex worker caste systems have contnbuted to the evolutionary success of advanced ant societies; however, little is known about the developmental processes underlying their origin and evolution. ...We combined hormonal manipulation, gene expression, and phylogenetic analyses with field observations to understand how novel worker subcastes evolve. We uncovered an ancestral developmental potential to produce a "supersoldier" subcaste that has been actualized at least two times independently in the hyperdiverse ant genus Pheidole. This potential has been retained and can be environmentally induced throughout the genus. Therefore, the retention and induction of this potential have facilitated the parallel evolution of supersoldiers through a process known as genetic accommodation. The recurrent induction of ancestral developmental potential may facilitate the adaptive and parallel evolution of phenotypes.
The genome of the fire ant Solenopsis invicta Wurm, Yannick; Wang, John; Riba-Grognuz, Oksana ...
Proceedings of the National Academy of Sciences - PNAS,
04/2011, Letnik:
108, Številka:
14
Journal Article
Recenzirano
Odprti dostop
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 5. 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 5. 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.
We study male parentage and between-colony variation in sex allocation and sexual production in the desert ant Crematogaster smithi, which usually has only one singly-mated queen per nest. Colonies ...of this species are known to temporarily store nutrients in the large fat body of intermorphs, a specialized female caste intermediate in morphology between queens and workers. Intermorphs repackage at least part of this fat into consumable but viable male-destined eggs. If these eggs sometimes develop instead of being eaten, intermorphs will be reproductive competitors of the queen but--due to relatedness asymmetries--allies of their sister worker. Using genetic markers we found a considerable proportion of non-queen sons in some, but not all, colonies. Even though intermorphs produce ∼1.7× more eggs than workers, their share in the parentage of adult males is estimated to be negligible due to their small number compared to workers. Furthermore, neither colony-level sex allocation nor overall sexual production was correlated with intermorph occurrence or number. We conclude that intermorph-laid eggs typically do not survive and that the storage of nutrients and their redistribution as eggs by intermorphs is effectively altruistic.
A remarkable social polymorphism is controlled by a single Mendelian factor in the fire ant Solenopsis invicta. A genomic element marked by the gene Gp‐9 determines whether workers tolerate one or ...many fertile queens in their colony. Gp‐9 was recently shown to be part of a supergene with two nonrecombining variants, SB and Sb. SB/SB and SB/Sb queens differ in how they initiate new colonies, and in many physiological traits, for example odour and maturation rate. To understand how a single genetic element can affect all these traits, we used a microarray to compare gene expression patterns between SB/SB and SB/Sb queens of three different age classes: 1‐day‐old unmated queens, 11‐day‐old unmated queens and mated, fully reproductive queens collected from mature field colonies. The number of genes that were differentially expressed between SB/SB and SB/Sb queens of the same age class was smallest in 1‐day‐old queens, maximal in 11‐day‐old queens and intermediate in reproductive queens. Gene ontology analysis showed that SB/SB queens upregulate reproductive genes faster than SB/Sb queens. For all age classes, genes inside the supergene were overrepresented among the differentially expressed genes. Consistent with the hypothesized greater number of transposons in the Sb supergene, 13 transposon genes were upregulated in SB/Sb queens. Viral genes were also upregulated in SB/Sb mature queens, consistent with the known greater parasite load in colonies headed by SB/Sb queens compared with colonies headed by SB/SB queens. Eighteen differentially expressed genes between reproductive queens were involved in chemical signalling. Our results suggest that many genes in the supergene are involved in regulating social organization and queen phenotypes in fire ants.
Workers of most eusocial Hymenoptera can produce sons but rarely do so in the presence of the queen, despite the potentially high fitness payoff of direct reproduction. It has often been suggested ...that colony-level productivity costs may outweigh the fitness advantages of worker reproduction, but this has never been shown. We estimated these costs in two ant species with large complex societies, the leafcutter ants
Acromyrmex echinatior and
Acromyrmex octospinosus, by splitting 16 laboratory colonies and comparing the dynamics of the fungus garden volume between orphaned and queenright nests (with and without laying workers, respectively). Apart from fungus volume as a longitudinal measure of colony productivity, we estimated sex allocation, the timing of the switch between raising queen offspring and worker sons, and differences in body mass between queen and worker sons. We showed that orphaned nests give priority to raising dispersing queen-derived sexuals (virgin queens, haploid and diploid queen sons) over raising worker sons. Worker sons could be heavier than, equally heavy as, or lighter than queen sons, depending on the condition of the colony. The reduction in colony productivity of orphaned nests compared to their queenright counterparts was negligible (≤1.2%), at least during the first 9 weeks after queen loss when these costs could be estimated. Such low costs could only outweigh the benefit of worker laying if the survival of worker sons is low, for example if workers show efficient worker policing, or discriminate against all male brood outside the brief reproductive season.
The fungal cultivars of fungus-growing ants are vertically transmitted by queens but not males. Selection would therefore favor cultivars that bias the ants' sex ratio towards gynes, beyond the gyne ...bias that is optimal for workers and queens. We measured sex allocation in 190 colonies of six sympatric fungus-growing ant species. As predicted from relatedness, female bias was greater in four singly mated Sericomyrmex and Trachymyrmex species than in two multiply mated Acromyrmex species. Colonies tended to raise mainly a single sex, which could be partly explained by variation in queen number, colony fecundity, and fungal garden volume for Acromyrmex and Sericomyrmex, but not for Trachymyrmex. Year of collection, worker number and mating frequency of Acromyrmex queens did not affect the colony sex ratios. We used a novel sensitivity analysis to compare the population sex allocation ratios with the theoretical queen and worker optima for a range of values of k, the correction factor for sex differences in metabolic rate and fat content. The results were consistent with either worker or queen control, but never with fungal control for any realistic value of k. We conclude that the fungal symbiont does not distort the ants' sex ratio in these species.
Understanding the relative evolutionary importance of parasites to different host taxa is problematic because the expression of disease and resistance are often confounded by factors such as host age ...and condition. The antibiotic-producing metapleural glands of ants are a potentially useful exception to this rule because they are a key first-line defense that are fixed in size in adults. Here we conduct a comparative analysis of the size of the gland reservoir across the fungus-growing ants (tribe Attini). Most attines have singly mated queens, but in two derived genera, the leaf-cutting ants, the queens are multiply mated, which is hypothesized to have evolved to improve colony-level disease resistance. We found that, relative to body size, the gland reservoirs of most attines are similar in size but that those of the leaf-cutting ants are significantly larger. In contrast, the size of the reservoir did not relate with the evolutionary transition from lower to higher attines and correlated at most only slightly with colony size. The results thus suggest that the relationship between leaf-cutting ants and their parasites is distinctly different from that for other attine ants, in accord with the hypothesis that multiple mating by queens evolved to improve colony-level disease resistance.
Nonreproductive workers of many eusocial Hymenoptera ‘police’ the colony, that is, they attack reproductive sister workers or destroy their eggs (unfertilized; developing into haploid males). Several ...ultimate causes of policing have been proposed, including (1) an increase in colony productivity, applicable if reproductive workers work less, or (2) an increase in worker-to-male relatedness, applicable if within-colony relatedness is low. To explain the distribution of policing across taxa, the explanatory power of these and other potential ultimate causes should be assessed separately. One of the few species for which this can be done is the leafcutter ant
Acromyrmex echinatior. We previously demonstrated that colony productivity incentives (and sex ratio incentives) are minimal here, while relatedness incentives are strong because queens are highly multiply mated. Overcoming technical difficulties peculiar to leafcutter ants, we introduced reproductive versus nonreproductive workers and batches of queen-laid versus worker-laid eggs into experimental colony fragments and observed their fate. Our main finding was that workers policed by selectively destroying worker-laid eggs, but without attacking reproductive workers. We infer that relatedness incentives are the most likely ultimate cause of the evolutionary maintenance of worker–egg policing in
A. echinatior.
Eusocial insects offer special opportunities for the comparative study of sperm traits because sperm competition is absent (in species with obligatory monandry) or constrained (in lineages where ...queens mate multiply but never remate later in life). We measured sperm length in 19 species of fungus-growing ants, representing 9 of the 12 recognized genera, and mapped these onto the ant phylogeny. We show that average sperm length across species is highly variable and decreases with mature colony size in basal genera with singly mated queens, suggesting that sperm production or storage constraints affect the evolution of sperm length. Sperm length does not decrease further in multiply mating leaf-cutting ants, despite substantial further increases in colony size. In a combined analysis, sexual dimorphism explained 63.1% of the variance in sperm length between species. As colony size was not a significant predictor in this analysis, we conclude that sperm production trade-offs in males have been the major selective force affecting sperm length across the fungus-growing ants, rather than storage constraints in females. The relationship between sperm length and sexual dimorphism remained robust in phylogenetically independent contrasts. Some of the remaining variation was explained by the relative size of the sperm-storage organ, but only in the multiply mating leaf-cutting ants, suggesting that sperm-storage constraints become important for the evolution of sperm length in this derived group. Mate number affected sperm length to a minor extent, and only in interaction with other predictor variables, suggesting that sperm competition has not been a major selective force for sperm length evolution in these ants.
We study male parentage and between-colony variation in sex allocation and sexual production in the desert ant Crematogaster smithi, which usually has only one singly-mated queen per nest. Colonies ...of this species are known to temporarily store nutrients in the large fat body of intermorphs, a specialized female caste intermediate in morphology between queens and workers. Intermorphs repackage at least part of this fat into consumable but viable male-destined eggs. If these eggs sometimes develop instead of being eaten, intermorphs will be reproductive competitors of the queen but-due to relatedness asymmetries-allies of their sister worker. Using genetic markers we found a considerable proportion of non-queen sons in some, but not all, colonies. Even though intermorphs produce ~1.7 more eggs than workers, their share in the parentage of adult males is estimated to be negligible due to their small number compared to workers. Furthermore, neither colony-level sex allocation nor overall sexual production was correlated with intermorph occurrence or number. We conclude that intermorph-laid eggs typically do not survive and that the storage of nutrients and their redistribution as eggs by intermorphs is effectively altruistic.
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