Recombination, chromosome number and eusociality in the Hymenoptera.
ABSTRACT: Extraordinarily high rates of recombination have been observed in some eusocial species. The most popular explanation is that increased recombination increases genetic variation among workers, which in turn increases colony performance, for example by increasing parasite resistance. However, support for the generality of higher recombination rates among eusocial organisms remains weak, due to low sample size and a lack of phylogenetic independence of observations. Recombination rate, although difficult to measure directly, is correlated with chromosome number. As predicted, several authors have noted that chromosome numbers are higher among the eusocial species of Hymenoptera (ants, bees and wasps). Here, we present a formal comparative analysis of karyotype data from 1567 species of Hymenoptera. Contrary to earlier studies, we find no evidence for an absolute difference between chromosome number in eusocial and solitary species of Hymenoptera. However, we find support for an increased rate of chromosome number change in eusocial taxa. We show that among eusocial taxa colony size is able to explain some of the variation in chromosome number: intermediate-sized colonies have more chromosomes than those that are either very small or very large. However, we were unable to detect effects of a number of other colony characteristics predicted to affect recombination rate - including colony relatedness and caste number. Taken together, our results support the view that a eusocial lifestyle has led to variable selection pressure for increased recombination rates, but that identifying the factors contributing to this variable selection will require further theoretical and empirical effort.
Project description:Around 150 million years ago, eusocial termites evolved from within the cockroaches, 50 million years before eusocial Hymenoptera, such as bees and ants, appeared. Here, we report the 2-Gb genome of the German cockroach, Blattella germanica, and the 1.3-Gb genome of the drywood termite Cryptotermes secundus. We show evolutionary signatures of termite eusociality by comparing the genomes and transcriptomes of three termites and the cockroach against the background of 16 other eusocial and non-eusocial insects. Dramatic adaptive changes in genes underlying the production and perception of pheromones confirm the importance of chemical communication in the termites. These are accompanied by major changes in gene regulation and the molecular evolution of caste determination. Many of these results parallel molecular mechanisms of eusocial evolution in Hymenoptera. However, the specific solutions are remarkably different, thus revealing a striking case of convergence in one of the major evolutionary transitions in biological complexity.
Project description:Queens and workers of eusocial Hymenoptera are considered homologous to the reproductive and brood care phases of an ancestral subsocial life cycle. However, the molecular mechanisms underlying the evolution of reproductive division of labor remain obscure. Using a brain transcriptomics screen, we identified a single gene, insulin-like peptide 2 (ilp2), which is always up-regulated in ant reproductives, likely because they are better nourished than their nonreproductive nestmates. In clonal raider ants (Ooceraea biroi), larval signals inhibit adult reproduction by suppressing ilp2, thus producing a colony reproductive cycle reminiscent of ancestral subsociality. However, increasing ILP2 peptide levels overrides larval suppression, thereby breaking the colony cycle and inducing a stable division of labor. These findings suggest a simple model for the origin of ant eusociality via nutritionally determined reproductive asymmetries potentially amplified by larval signals.
Project description:Eusocial insects, mostly Hymenoptera, have evolved unique colonial lifestyles that rely on the perception of social context mainly through pheromones, and chemoreceptors are hypothesized to have played important adaptive roles in the evolution of sociality. However, because chemoreceptor repertoires have been characterized in few social insects and their solitary relatives, a comprehensive examination of this hypothesis has not been possible. Here, we annotate ?3,000 odorant and gustatory receptors in recently sequenced Hymenoptera genomes and systematically compare >4,000 chemoreceptors from 13 hymenopterans, representing one solitary lineage (wasps) and three independently evolved eusocial lineages (ants and two bees). We observe a strong general tendency for chemoreceptors to expand in Hymenoptera, whereas the specifics of gene gains/losses are highly diverse between lineages. We also find more frequent positive selection on chemoreceptors in a facultative eusocial bee and in the common ancestor of ants compared with solitary wasps. Our results suggest that the frequent expansions of chemoreceptors have facilitated the transition to eusociality. Divergent expression patterns of odorant receptors between honeybee and ants further indicate differential roles of chemoreceptors in parallel trajectories of social evolution.
Project description:Eusocial organisms are characterized by cooperative brood care, generation overlap and reproductive division of labour. Traits associated with eusociality are most developed in ants, termites, paper wasps and corbiculate bees; the fossil record indicates that each of these advanced eusocial taxa evolved in the Late Cretaceous or earlier (greater than 65 Myr ago). Halictid bees also include a large and diverse number of eusocial members, but, in contrast to advanced eusocial taxa, they are characterized by substantial intra- and inter-specific variation in social behaviour, which may be indicative of more recent eusocial evolution. To test this hypothesis, we used over 2400 bp of DNA sequence data gathered from three protein-coding nuclear genes (opsin, wingless and EF-1a) to infer the phylogeny of eusocial halictid lineages and their relatives. Results from relaxed molecular clock dating techniques that utilize a combination of molecular and fossil data indicate that the three independent origins of eusociality in halictid bees occurred within a narrow time frame between approximately 20 and 22 Myr ago. This relatively recent evolution helps to explain the pronounced levels of social variation observed within these bees. The three origins of eusociality appear to be temporally correlated with a period of global warming, suggesting that climate may have had an important role in the evolution and maintenance of eusociality in these bees.
Project description:Explaining the evolution of sex and recombination is particularly intriguing for some species of eusocial insects because they display exceptionally high mating frequencies and genomic recombination rates. Explanations for both phenomena are based on the notion that both increase colony genetic diversity, with demonstrated benefits for colony disease resistance and division of labor. However, the relative contributions of mating number and recombination rate to colony genetic diversity have never been simultaneously assessed. Our study simulates colonies, assuming different mating numbers, recombination rates, and genetic architectures, to assess their worker genotypic diversity. The number of loci has a strong negative effect on genotypic diversity when the allelic effects are inversely scaled to locus number. In contrast, dominance, epistasis, lethal effects, or limiting the allelic diversity at each locus does not significantly affect the model outcomes. Mating number increases colony genotypic variance and lowers variation among colonies with quickly diminishing returns. Genomic recombination rate does not affect intra- and inter-colonial genotypic variance, regardless of mating frequency and genetic architecture. Recombination slightly increases the genotypic range of colonies and more strongly the number of workers with unique allele combinations across all loci. Overall, our study contradicts the argument that the exceptionally high recombination rates cause a quantitative increase in offspring genotypic diversity across one generation. Alternative explanations for the evolution of high recombination rates in social insects are therefore needed. Short-term benefits are central to most explanations of the evolution of multiple mating and high recombination rates in social insects but our results also apply to other species.
Project description:Halictine sweat bees (Hymenoptera, Halictidae) are model organisms for the evolution of altruism, reproductive castes, and eusocial colony organization. Halictine social behavior is not only extremely variable, but also ecologically and evolutionarily labile. Among social species, colony social organization ranges from communal societies of egalitarian females to eusocial and semisocial ones with reproductive queens and more or less sterile workers. A striking aspect of halictine social variation is the mutual exclusivity of communal and eusocial types of colony social organization within the same species, these two types of social behavior being characteristic of different genera and subgenera. We report a recently discovered exception to this rule in a population of Halictus sexcinctus (Fabricius) at Daimonia-Pyla in southern Greece, that contained both communal and eusocial colonies. Moreover, communal and eusocial females exhibit morphological differences that imply a preimaginal developmental switch, which could also underlie the two types of social behavior. That the communal and eusocial forms are not merely cryptic sister species with different social behavior is indicated by the comparison of mitochondrial DNA sequences of two sections of cytochrome oxidase I, which indicate that Greek specimens of both social types are more similar than they are to conspecifics from elsewhere in Europe. The phylogenetic position of Halictus sexcinctus suggests that this unusual communal/eusocial polymorphism may represent an unstable intermediate step in an evolutionary reversal from eusocial to solitary behavior.
Project description:Changes in gene regulation that underlie phenotypic evolution can be encoded directly in the DNA sequence or mediated by chromatin modifications such as DNA methylation. It has been hypothesized that the evolution of eusocial division of labor is associated with enhanced gene regulatory potential, which may include expansions in DNA methylation in the genomes of Hymenoptera (bees, ants, wasps, and sawflies). Recently, this hypothesis garnered support from analyses of a commonly used metric to estimate DNA methylation in silico, CpG content. Here, we test this hypothesis using direct, nucleotide-level measures of DNA methylation across nine species of Hymenoptera. In doing so, we generated new DNA methylomes for three species of interest, including one solitary and one facultatively eusocial halictid bee and a sawfly. We demonstrate that the strength of correlation between CpG content and DNA methylation varies widely among hymenopteran taxa, highlighting shortcomings in the utility of CpG content as a proxy for DNA methylation in comparative studies of taxa with sparse DNA methylomes. We observed strikingly high levels of DNA methylation in the sawfly relative to other investigated hymenopterans. Analyses of molecular evolution suggest the relatively distinct sawfly DNA methylome may be associated with positive selection on functional DNMT3 domains. Sawflies are an outgroup to all ants, bees, and wasps, and no sawfly species are eusocial. We find no evidence that either global expansions or variation within individual ortholog groups in DNA methylation are consistently associated with the evolution of social behavior.
Project description:The remarkably high level of colony organization found in the honey bees and stingless bees (family Apidae) is extremely rare among animals. Yet there is controversy over whether these two groups independently evolved advanced eusocial behavior or inherited it from a common ancestor. Phylogenetic analyses of DNA sequence information from the mitochondrial genome (large-subunit ribosomal RNA gene) of representative apid bees suggest that advanced eusocial behavior evolved twice independently within this assemblage. These results depart from previous hypotheses of apid relationships by indicating a close phylogenetic relationship between the primitively eusocial bumble bees and the stingless bees.
Project description:Explaining the origin of eusociality, with strict division of labour between workers and reproductives, remains one of evolutionary biology's greatest challenges. Specific combinations of genetic, behavioural and demographic traits in Hymenoptera are thought to explain their relatively high frequency of eusociality, but quantitative models integrating such preadaptations are lacking. Here we use mathematical models to show that the joint evolution of helping behaviour and maternal sex ratio adjustment can synergistically trigger both a behavioural change from solitary to eusocial breeding, and a demographic change from a life cycle with two reproductive broods to a life cycle in which an unmated cohort of female workers precedes a final generation of dispersing reproductives. Specific suits of preadaptations are particularly favourable to the evolution of eusociality: lifetime monogamy, bivoltinism with male generation overlap, hibernation of mated females and haplodiploidy with maternal sex ratio adjustment. The joint effects of these preadaptations may explain the abundance of eusociality in the Hymenoptera and its virtual absence in other haplodiploid lineages.
Project description:Ants (Hymenoptera, Formicidae) represent one of the most successful eusocial taxa in terms of both their geographic distribution and species number. The publication of seven ant genomes within the past year was a quantum leap for socio- and ant genomics. The diversity of social organization in ants makes them excellent model organisms to study the evolution of social systems. Comparing the ant genomes with those of the honeybee, a lineage that evolved eusociality independently from ants, and solitary insects suggests that there are significant differences in key aspects of genome organization between social and solitary insects, as well as among ant species. Altogether, these seven ant genomes open exciting new research avenues and opportunities for understanding the genetic basis and regulation of social species, and adaptive complex systems in general.