Sociality sculpts similar patterns of molecular evolution in two independently evolved lineages of eusocial bees.
Ontology highlight
ABSTRACT:
SUBMITTER: Shell WA
PROVIDER: S-EPMC7977082 | biostudies-literature |
REPOSITORIES: biostudies-literature
Similar Datasets
Project description:Eusociality is a major evolutionary innovation involving alterations in life history, morphology, and behavior. Advanced eusocial insects, such as ants, termites, and corbiculate bees, cannot provide insights into the earliest stages of eusocial evolution because eusociality in these taxa evolved long ago (in the Cretaceous) and close solitary relatives are no longer extant. In contrast, primitively eusocial insects, such as halictid bees, provide insights into the early stages of eusocial evolution because eusociality has arisen recently and repeatedly. By mapping social behavior onto well-corroborated phylogenies, I show that eusociality has arisen only three times within halictid bees (contrary to earlier estimates of six or more origins). Reversals from eusocial to solitary behavior have occurred as many as 12 times, indicating that social reversals are common in the earliest stages of eusocial evolution. Important attributes of social complexity (e.g., colony size, queen/worker dimorphism) show no obvious association with phylogeny, and some reversals to solitary nesting are related to host-plant switches (from polylecty to oligolecty). These results provide a glimpse of social evolution in its earliest stages and provide insights into the early evolution of advanced eusocial organisms.
| S-EPMC117553 | biostudies-literature
Project description:BackgroundSociality has many rewards, but can also be dangerous, as high population density and low genetic diversity, common in social insects, is ideal for parasite transmission. Despite this risk, honeybees and other sequenced social insects have far fewer canonical immune genes relative to solitary insects. Social protection from infection, including behavioral responses, may explain this depauperate immune repertoire. Here, based on full genome sequences, we describe the immune repertoire of two ecologically and commercially important bumblebee species that diverged approximately 18 million years ago, the North American Bombus impatiens and European Bombus terrestris.ResultsWe find that the immune systems of these bumblebees, two species of honeybee, and a solitary leafcutting bee, are strikingly similar. Transcriptional assays confirm the expression of many of these genes in an immunological context and more strongly in young queens than males, affirming Bateman's principle of greater investment in female immunity. We find evidence of positive selection in genes encoding antiviral responses, components of the Toll and JAK/STAT pathways, and serine protease inhibitors in both social and solitary bees. Finally, we detect many genes across pathways that differ in selection between bumblebees and honeybees, or between the social and solitary clades.ConclusionsThe similarity in immune complement across a gradient of sociality suggests that a reduced immune repertoire predates the evolution of sociality in bees. The differences in selection on immune genes likely reflect divergent pressures exerted by parasites across social contexts.
| S-EPMC4408586 | biostudies-literature
Project description:The social brain hypothesis (SBH) posits that the demands imposed on individuals by living in cohesive social groups exert a selection pressure favouring the evolution of large brains and complex cognitive abilities. Using volumetry and the isotropic fractionator to determine the size of and numbers of neurons in specific brain regions, here we test this hypothesis in African mole-rats (Bathyergidae). These subterranean rodents exhibit a broad spectrum of social complexity, ranging from strictly solitary through to eusocial cooperative breeders, but feature similar ecologies and life history traits. We found no positive association between sociality and neuroanatomical correlates of information-processing capacity. Solitary species are larger, tend to have greater absolute brain size and have more neurons in the forebrain than social species. The neocortex ratio and neuronal counts correlate negatively with social group size. These results are clearly inconsistent with the SBH and show that the challenges coupled with sociality in this group of rodents do not require brain enlargement or fundamental reorganization. These findings suggest that group living or pair bonding per se does not select strongly for brain enlargement unless coupled with Machiavellian interactions affecting individual fitness.
| S-EPMC6003933 | biostudies-literature
Project description:Some of the fastest evolving regions of the human genome are conserved noncoding elements with many human-specific DNA substitutions. These human accelerated regions (HARs) are enriched nearby regulatory genes, and several HARs function as developmental enhancers. To investigate if this evolutionary signature is unique to humans, we quantified evidence of accelerated substitutions in conserved genomic elements across multiple lineages and applied this approach simultaneously to the genomes of five apes: human, chimpanzee, gorilla, orangutan, and gibbon. We find roughly similar numbers and genomic distributions of lineage-specific accelerated regions (linARs) in all five apes. In particular, apes share an enrichment of linARs in regulatory DNA nearby genes involved in development, especially transcription factors and other regulators. Many developmental loci harbor clusters of nonoverlapping linARs from multiple apes, suggesting that accelerated evolution in each species affected distinct regulatory elements that control a shared set of developmental pathways. Our statistical tests distinguish between GC-biased and unbiased accelerated substitution rates, allowing us to quantify the roles of different evolutionary forces in creating linARs. We find evidence of GC-biased gene conversion in each ape, but unbiased acceleration consistent with positive selection or loss of constraint is more common in all five lineages. It therefore appears that similar evolutionary processes created independent accelerated regions in the genomes of different apes, and that these lineage-specific changes to conserved noncoding sequences may have differentially altered expression of a core set of developmental genes across ape evolution.
| S-EPMC6063267 | biostudies-literature
Project description:Understanding the ecological and environmental contexts in which eusociality can evolve is fundamental to elucidating its evolutionary origins. A sufficiently long active season is postulated to have been a key factor facilitating the transition to eusociality. Many primitively eusocial species exhibit an annual life cycle, which is thought to preclude the expression of eusociality where the active season is too short to produce successive worker and reproductive broods. However, few studies have attempted to test this idea experimentally. We investigated environmental constraints on the expression of eusociality in the obligate primitively eusocial sweat bee Lasioglossum malachurum, by transplanting nest foundresses from the south to the far north of the United Kingdom, far beyond the natural range of L. malachurum. We show that transplanted bees can exhibit eusociality, but that the short length of the season and harsher environmental conditions could preclude its successful expression. In one year, when foundresses were transplanted only after provisioning first brood (B1) offspring, workers emerged in the north and provisioned a second brood (B2) of reproductives. In another year, when foundresses were transplanted prior to B1 being provisioned, they were just as likely to initiate nesting and provisioned just as many B1 cells as foundresses in the south. However, the life cycle was delayed by approximately 7 weeks and nests suffered 100% B1 mortality. Our results suggest that short season length together with poor weather conditions represent an environmental barrier to the evolution and expression of eusociality in sweat bees.
| S-EPMC6208632 | biostudies-literature
Project description:Eusocial insects offer a unique opportunity to analyze the evolution of body size differences between sexes in relation to social environment. The workers, being sterile females, are not subject to selection for reproductive function providing a natural control for parsing the effects of selection on reproductive function (i.e., sexual and fecundity selection) from other kinds of natural selection. Patterns of sexual size dimorphism (SSD) and testing of Rensch's rule controlling for phylogenetic effects were analyzed in the Meliponini or stingless bees. Theory predicts that queens may exhibit higher selection for fecundity in eusocial taxa, but contrary to this, we found mixed patterns of SSD in Meliponini. Non-Melipona species generally have a female-biased SSD, while all analyzed species of Melipona showed a male-biased SSD, indicating that the direction and magnitude of the selective pressures do not operate in the same way for all members of this taxon. The phylogenetic regressions revealed that the rate of divergence has not differed between the two castes of females and the males, that is, stingless bees do not seem to follow Rensch's rule (a slope >1), adding this highly eusocial taxon to the various solitary insect taxa not conforming with it. Noteworthy, when Melipona was removed from the analysis, the phylogenetic regressions for the thorax width of males on queens had a slope significantly smaller than 1, suggesting that the evolutionary divergence has been larger in queens than males, and could be explained by stronger selection on female fecundity only in non-Melipona species. Our results in the stingless bees question the classical explanation of female-biased SSD via fecundity and provide a first evidence of a more complex determination of SSD in highly eusocial species. We suggest that in highly eusocial taxa, additional selection mechanisms, possibly related to individual and colonial interests, could influence the evolution of environmentally determined traits such as body size.
| S-EPMC6405504 | biostudies-literature
Project description:Evidence for the antiquity and importance of microbial pathogens as selective agents is found in the proliferation of antimicrobial defences throughout the animal kingdom. Social insects, typified by crowding and often by low genetic variation, have high probabilities of disease transmission and eusocial Hymenoptera may be particularly vulnerable because of haplodiploidy. Mechanisms they employ to reduce the risk of disease include antimicrobial secretions which are particularly important primary barriers to infection. However, until now, whether or not there is selection for stronger antimicrobial secretions when the risk of disease increases because of sociality has not been tested. Here, we present evidence that the production of progressively stronger antimicrobial compounds was critical to the evolution of sociality in bees. We found that increases in group size and genetic relatedness were strongly correlated with increasing antimicrobial strength. The antimicrobials of even the most primitive semi-social species were an order of magnitude stronger that those of solitary species, suggesting a point of no return, beyond which disease control was essential. Our results suggest that selection by microbial pathogens was critical to the evolution of sociality and required the production of strong, front-line antimicrobial defences.
| S-EPMC2390670 | biostudies-literature
Project description:Marine sediments represent a vast habitat for complex microbiomes. Among these, ammonia oxidizing archaea (AOA) of the phylum Thaumarchaeota are one of the most common, yet little explored, inhabitants, which seem extraordinarily well adapted to the harsh conditions of the subsurface biosphere. We present 11 metagenome-assembled genomes of the most abundant AOA clades from sediment cores obtained from the Atlantic Mid-Ocean ridge flanks and Pacific abyssal plains. Their phylogenomic placement reveals three independently evolved clades within the order Nitrosopumilales, of which no cultured representative is known yet. In addition to the gene sets for ammonia oxidation and carbon fixation known from other AOA, all genomes encode an extended capacity for the conversion of fermentation products that can be channeled into the central carbon metabolism, as well as uptake of amino acids probably for protein maintenance or as an ammonia source. Two lineages encode an additional (V-type) ATPase and a large repertoire of DNA repair systems that may allow to overcome the challenges of high hydrostatic pressure. We suggest that the adaptive radiation of AOA into marine sediments occurred more than once in evolution and resulted in three distinct lineages with particular adaptations to this extremely energy-limiting and high-pressure environment.
| S-EPMC8397731 | biostudies-literature
Project description:Understanding how alternative phenotypes arise from the same genome is a major challenge in modern biology. Eusociality in insects requires the evolution of two alternative phenotypes - workers, who sacrifice personal reproduction, and queens, who realize that reproduction. Extensive work on honeybees and ants has revealed the molecular basis of derived queen and worker phenotypes in highly eusocial lineages, but we lack equivalent deep-level analyses of wasps and of primitively eusocial species, the latter of which can reveal how phenotypic decoupling first occurs in the early stages of eusocial evolution.We sequenced 20 Gbp of transcriptomes derived from brains of different behavioral castes of the primitively eusocial tropical paper wasp Polistes canadensis. Surprisingly, 75% of the 2,442 genes differentially expressed between phenotypes were novel, having no significant homology with described sequences. Moreover, 90% of these novel genes were significantly upregulated in workers relative to queens. Differential expression of novel genes in the early stages of sociality may be important in facilitating the evolution of worker behavioral complexity in eusocial evolution. We also found surprisingly low correlation in the identity and direction of expression of differentially expressed genes across similar phenotypes in different social lineages, supporting the idea that social evolution in different lineages requires substantial de novo rewiring of molecular pathways.These genomic resources for aculeate wasps and first transcriptome-wide insights into the origin of castes bring us closer to a more general understanding of eusocial evolution and how phenotypic diversity arises from the same genome.
| S-EPMC4053794 | biostudies-literature
Project description:Fungi that have the enzymes cyanase and carbonic anhydrase show a limited capacity to detoxify cyanate, a fungicide employed by both plants and humans. Here, we describe a novel two-gene cluster that comprises duplicated cyanase and carbonic anhydrase copies, which we name the CCA gene cluster, trace its evolution across Ascomycetes, and examine the evolutionary dynamics of its spread among lineages of the Fusarium oxysporum species complex (hereafter referred to as the FOSC), a cosmopolitan clade of purportedly clonal vascular wilt plant pathogens. Phylogenetic analysis of fungal cyanase and carbonic anhydrase genes reveals that the CCA gene cluster arose independently at least twice and is now present in three lineages, namely Cochliobolus lunatus, Oidiodendron maius, and the FOSC. Genome-wide surveys within the FOSC indicate that the CCA gene cluster varies in copy number across isolates, is always located on accessory chromosomes, and is absent in FOSC's closest relatives. Phylogenetic reconstruction of the CCA gene cluster in 163 FOSC strains from a wide variety of hosts suggests a recent history of rampant transfers between isolates. We hypothesize that the independent formation of the CCA gene cluster in different fungal lineages and its spread across FOSC strains may be associated with resistance to plant-produced cyanates or to use of cyanate fungicides in agriculture.
| S-EPMC4438557 | biostudies-literature