Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.

Genetics and analysis of quantitative traits

In his introduction to this detailed survey of knowledge of insect societies, the author points out that research on insect sociology has proceeded in three phases, the natural history phase, the physiological phase and the population-biology phase. Advances in the first two phases have permitted embarkation in the third phase on a more rigorous theory of social evolution based on population genetics and writing this book, the author wished to relate the three phases of research on insects and to express insect sociology as population biology. A glossary of terms, a considerable bibliography and a general index are included. Other CABI sites 

The Insect Societies

Long non-coding RNAs (lncRNAs) are diverse transcription products emanating from thousands of loci in mammalian genomes. Cis-acting lncRNAs, which constitute a substantial fraction of lncRNAs with an attributed function, regulate gene expression in a manner dependent on the location of their own sites of transcription, at varying distances from their targets in the linear genome. Through various mechanisms, cis-acting lncRNAs have been demonstrated to activate, repress or otherwise modulate the expression of target genes. We discuss the activities that have been ascribed to cis-acting lncRNAs, the evidence and hypotheses regarding their modes of action, and the methodological advances that enable their identification and characterization. The emerging principles highlight lncRNAs as transcriptional units highly adept at contributing to gene regulatory networks and to the generation of fine-tuned spatial and temporal gene expression programmes.

Regulation of gene expression by cis-acting long non-coding RNAs.

The domestication of plants and animals over the past 11,500 years has had a significant effect not just on the domesticated taxa but also on human evolution and on the biosphere as a whole. Decades of research into the geographical and chronological origins of domestic animals have led to a general understanding of the pattern and process of domestication, though a number of significant questions remain unresolved. Here, building upon recent theoretical advances regarding the different pathways animals followed to become domesticated, we present a large-scale synthesis that addresses the global pattern of animal domestication alongside a discussion of the differential evolutionary processes that have shaped domestic animal populations. More specifically, we present a framework for understanding how unconscious selection characterized the earliest steps of animal domestication and the role of introgression and the importance of relaxed and positive selection in shaping modern domestic phenotypes and genomes.

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The Evolution of Animal Domestication

Most theories used to explain the evolution of eusociality rest upon two key assumptions: mutations affecting the phenotype of sterile workers evolve by positive selection if the resulting traits benefit fertile kin, and that worker traits provide the primary mechanism allowing social insects to adapt to their environment. Despite the common view that positive selection drives phenotypic evolution of workers, we know very little about the prevalence of positive selection acting on the genomes of eusocial insects. We mapped the footprints of positive selection in Apis mellifera through analysis of 40 individual genomes, allowing us to identify thousands of genes and regulatory sequences with signatures of adaptive evolution over multiple timescales. We found Apoidea- and Apis-specific genes to be enriched for signatures of positive selection, indicating that novel genes play a disproportionately large role in adaptive evolution of eusocial insects. Worker-biased proteins have higher signatures of adaptive evolution relative to queen-biased proteins, supporting the view that worker traits are key to adaptation. We also found genes regulating worker division of labor to be enriched for signs of positive selection. Finally, genes associated with worker behavior based on analysis of brain gene expression were highly enriched for adaptive protein and cis-regulatory evolution. Our study highlights the significant contribution of worker phenotypes to adaptive evolution in social insects, and provides a wealth of knowledge on the loci that influence fitness in honey bees.

https://www.pnas.org/content/pnas/111/7/2614.full.pdf

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits.

The process of domestication often brings about profound changes in levels of genetic variation in animals and plants. The honey bee, Apis mellifera, has been managed by humans for centuries for both honey and wax production and crop pollination. Human management and selective breeding are believed to have caused reductions in genetic diversity in honey bee populations, thereby contributing to the global declines threatening this ecologically and economically important insect. However, previous studies supporting this claim mostly relied on population genetic comparisons of European and African (or Africanized) honey bee races; such conclusions require reassessment given recent evidence demonstrating that the honey bee originated in Africa and colonized Europe via two independent expansions. We sampled honey bee workers from two managed populations in North America and Europe as well as several old-world progenitor populations in Africa, East and West Europe. Managed bees had highly introgressed genomes representing admixture between East and West European progenitor populations. We found that managed honey bees actually have higher levels of genetic diversity compared with their progenitors in East and West Europe, providing an unusual example whereby human management increases genetic diversity by promoting admixture. The relationship between genetic diversity and honey bee declines is tenuous given that managed bees have more genetic diversity than their progenitors and many viable domesticated animals.

Management Increases Genetic Diversity of Honey Bees via Admixture

The rise of insect societies, marked by the formation of reproductive and sterile castes, represents a major unsolved mystery in evolution. Across several independent origins of sociality, the genomes of social hymenopterans share two peculiar attributes: high recombination and low but heterogeneous GC content. For example, the genome of the honey bee, Apis mellifera, represents a mosaic of GC-poor and GC-rich regions with rates of recombination an order of magnitude higher than in humans. However, it is unclear how heterogeneity in GC content arises, and how it relates to the expression and evolution of worker traits. Using population genetic analyses, we demonstrate a bias in the allele frequency and fixation rate of derived C or G mutations in high-recombination regions, consistent with recombination’s causal influence on GC-content evolution via biased gene conversion. We also show that recombination and biased gene conversion actively maintain the heterogeneous GC content of the honey bee genome despite an overall A/T mutation bias. Further, we found that GC-rich genes and intergenic regions have higher levels of genetic diversity and divergence relative to GC-poor regions, also consistent with recombination’s causal influence on the rate of molecular evolution. Finally, we found that genes associated with behavior and those with worker-biased expression are found in GC-rich regions of the bee genome and also experience high rates of molecular evolution. Taken together, these findings suggest that recombination acts to maintain a genetically diverse and dynamic part of the genome where genes underlying worker behavior evolve more quickly.

https://www.pnas.org/content/pnas/109/44/18012.full.pdf

Recombination is associated with the evolution of genome structure and worker behavior in honey bees

Complementary sex determination is the ancestral sex-determination mechanism in the Hymenoptera.Underthissystem,diploidindividualsdevelopintofemalesiftheyareheterozygous atanautosomal sex-determininglocus orloci,whereas haploidindividualsdevelopintomales becausetheyare hemizygous at thesex-determininglocusorloci. However,diploidmales canstillarisefromfertilized eggs if such individuals are homozygous at the sex-determining locus or loci. Diploid males are often viable but sire few daughters, thereby representing a substantial genetic load in hymenopteran populations. Here, we review the effects of complementary sex determination and diploid male production from the perspective of female hymenopterans. Because female hymenopterans need not mate to produce haploid sons, complementary sex determination can cause special forms of mating failures by preventing some females from controlling the sex ratio of their brood and producing the desired number of daughters. Under some circumstances, complementary sex determination can cause complete mating failure by preventing females fromproducing daughters altogether. Although we outline serious gaps of knowledge in the field, the data at hand suggest that diploid male production can substantially increase mating failures in small populations of economically and ecologically important hymenopterans.

https://onlinelibrary.wiley.com/doi/pdf/10.1111/j.1570-7458.2012.01306.x

A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera

The genomes of eusocial insects have a reduced complement of immune genes-an unusual finding considering that sociality provides ideal conditions for disease transmission. The following three hypotheses have been invoked to explain this finding: 1) social insects are attacked by fewer pathogens, 2) social insects have effective behavioral or 3) novel molecular mechanisms for combating pathogens. At the molecular level, these hypotheses predict that canonical innate immune pathways experience a relaxation of selective constraint. A recent study of several innate immune genes in ants and bees showed a pattern of accelerated amino acid evolution, which is consistent with either positive selection or a relaxation of constraint. We studied the population genetics of innate immune genes in the honey bee Apis mellifera by partially sequencing 13 genes from the bee's Toll pathway (∼10.5 kb) and 20 randomly chosen genes (∼16.5 kb) sequenced in 43 diploid workers. Relative to the random gene set, Toll pathway genes had significantly higher levels of amino acid replacement mutations segregating within A. mellifera and fixed between A. mellifera and A. cerana. However, levels of diversity and divergence at synonymous sites did not differ between the two gene sets. Although we detect strong signs of balancing selection on the pathogen recognition gene pgrp-sa, many of the genes in the Toll pathway show signatures of relaxed selective constraint. These results are consistent with the reduced complement of innate immune genes found in social insects and support the hypothesis that some aspect of eusociality renders canonical innate immunity superfluous.

Brock A. Harpur

Papers

Population genomics of the honey bee reveals strong signatures of positive selection on worker traits.

Management Increases Genetic Diversity of Honey Bees via Admixture

Recombination is associated with the evolution of genome structure and worker behavior in honey bees

A review of the consequences of complementary sex determination and diploid male production on mating failures in the Hymenoptera

Accelerated Evolution of Innate Immunity Proteins in Social Insects: Adaptive Evolution or Relaxed Constraint?