We have estimated phylogenies of fungus-growing termites and their associated mutualistic fungi of the genus Termitomyces using Bayesian analyses of DNA sequences. Our study shows that the symbiosis has a single African origin and that secondary domestication of other fungi or reversal of mutualistic fungi to a freeliving state has not occurred. Host switching has been frequent, especially at the lower taxonomic levels, and nests of single termite , is derived with two independent origins. Despite repeated host switching, statistical tests taking phylogenetic uncertainty into account show a significant congruence between the termite and fungal phylogenies, because mutualistic interactions at higher taxonomic levels show considerable specificity. We identify common characteristics of fungus-farming evolution in termites and ants, which apply despite the major differences between these two insect agricultural systems. We hypothesize that biparental colony founding may have constrained the evolution of vertical symbiont transmission in termites but not in ants where males die after mating.
All evidence currently available indicates that obligatory sterile eusocial castes only arose via the association of lifetime monogamous parents and offspring. This is consistent with Hamilton's rule (br s . r o c), but implies that relatedness cancels out of the equation because average relatedness to siblings (r s ) and offspring (r o ) are both predictably 0.5. This equality implies that any infinitesimally small benefit of helping at the maternal nest (b), relative to the cost in personal reproduction (c) that persists throughout the lifespan of entire cohorts of helpers suffices to establish permanent eusociality, so that group benefits can increase gradually during, but mostly after the transition. The monogamy window can be conceptualized as a singularity comparable with the single zygote commitment of gametes in eukaryotes. The increase of colony size in ants, bees, wasps and termites is thus analogous to the evolution of multicellularity. Focusing on lifetime monogamy as a universal precondition for the evolution of obligate eusociality simplifies the theory and may help to resolve controversies about levels of selection and targets of adaptation. The monogamy window underlines that cooperative breeding and eusociality are different domains of social evolution, characterized by different sectors of parameter space for Hamilton's rule.
Pair formation in social insects mostly happens early in adult life and away from the social colony context, which precludes promiscuity in the usual sense. Termite males have continuous sperm production, but males of social Hymenoptera have fixed complements of sperm, except for a few species that mate before female dispersal and show male-fighting and lifelong sperm production. We develop an evolutionary framework for testing sexual selection and sperm competition theory across the advanced eusocial insects (ants, wasps, bees, termites) and highlight two areas related to premating sexual selection (sexual dimorphism and male mate number) that have remained understudied and in which considerable progress can be achieved with relatively simple approaches. We also infer that mating plugs may be relatively common, and we review further possibilities for postmating sexual selection, which gradually become less likely in termite evolution, but for which eusocial Hymenoptera provide unusual opportunities because they have clonal ejaculates and store viable sperm for up to several decades.
Termites normally rely on gut symbionts to decompose organic matter but the Macrotermitinae domesticated Termitomyces fungi to produce their own food. This transition was accompanied by a shift in the composition of the gut microbiota, but the complementary roles of these bacteria in the symbiosis have remained enigmatic. We obtained high-quality annotated draft genomes of the termite Macrotermes natalensis, its Termitomyces symbiont, and gut metagenomes from workers, soldiers, and a queen. We show that members from 111 of the 128 known glycoside hydrolase families are represented in the symbiosis, that Termitomyces has the genomic capacity to handle complex carbohydrates, and that worker gut microbes primarily contribute enzymes for final digestion of oligosaccharides. This apparent division of labor is consistent with the Macrotermes gut microbes being most important during the second passage of comb material through the termite gut, after a first gut passage where the crude plant substrate is inoculated with Termitomyces asexual spores so that initial fungal growth and polysaccharide decomposition can proceed with high efficiency. Complex conversion of biomass in termite mounds thus appears to be mainly accomplished by complementary cooperation between a domesticated fungal monoculture and a specialized bacterial community. In sharp contrast, the gut microbiota of the queen had highly reduced plant decomposition potential, suggesting that mature reproductives digest fungal material provided by workers rather than plant substrate.carbohydrate-active enzymes | eusocial | symbioses | cellulose | lignin
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.social insect | caste differences | nonmodel organism | de novo genome assembly
Sociality can be associated with significant costs due to the increased risk of disease transmission. However, in some organisms the costs may be offset by benefits due to improvements in defences against parasites. To examine this possible trade-off between infection risk and disease resistance, we used Acromyrmex leaf-cutting ants and the entomopathogenic fungus Metarhizium anisopliae as the model system. Ants exposed to the parasite were found to have substantially improved survival when they were kept with nest-mates, while the cost of being in a group in terms of increased disease transmission was very low. The efficiency of transmission is described by the transmission parameter, which decreased with increasing host density showing that transmission rates are inversely density dependent. Both grooming and antibiotic secretions appeared to be important in resistance against the parasite, with the defences of small workers being particularly effective. The results indicate that leaf-cutting ant colonies may have much greater resistance to disease than would be predicted from the high densities of host individuals within them. Unlike most organisms, group living in these ants may actually be associated with a net benefit in terms of disease dynamics.
I redevelop the hypothesis that lifetime monogamy is a fundamental condition for the evolution of eusocial lineages with permanent non-reproductive castes, and that later elaborations--such as multiply-mated queens and multi-queen colonies--arose without the re-mating promiscuity that characterizes non-social and cooperative breeding. Sexually selected traits in eusocial lineages are therefore peculiar, and their evolution constrained. Indirect (inclusive) fitness benefits in cooperatively breeding vertebrates appear to be negatively correlated with promiscuity, corroborating that kin selection and sexual selection tend to generally exclude each other. The monogamy window required for transitions from solitary and cooperative breeding towards eusociality implies that the relatedness and benefit-cost variables of Hamilton's rule do not vary at random, but occur in distinct and only partly overlapping combinations in cooperative, eusocial, and derived eusocial breeding systems.
Attine ants engage in a quadripartite symbiosis with fungi they cultivate for food, specialized garden parasites, and parasite-inhibiting bacteria. Molecular phylogenetic evidence supports an ancient host-pathogen association between the ant-cultivar mutualism and the garden parasite. Here we show that ants rear the antibiotic-producing bacteria in elaborate cuticular crypts, supported by unique exocrine glands, and that these structures have been highly modified across the ants' evolutionary history. This specialized structural evolution, together with the absence of these bacteria and modifications in other ant genera that do not grow fungus, indicate that the bacteria have an ancient and coevolved association with the ants, their fungal cultivar, and the garden parasite.
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