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Heterosis occurs in individuals when genetic diversity, i.e., heterozygosity, increases fitness. Many advanced eusocial insects evolved mating behaviors, including polyandry and polygyny, which increase inter-individual genetic diversity within colonies. The possibility of this structure of diversity to improve group fitness has been termed social heterosis. Neither the independence of individual and social heterosis nor their relative effect sizes have been explicitly measured. Through controlled breeding between pairs of Western honey bee queens (Apis mellifera L.; n=3 pairs) from two distinct populations, we created inbred colonies with low genetic diversity, hybrid colonies with high heterozygosity, and mixed colonies (combining inbred workers from each population) with low heterozygosity and high social diversity. We then quantified two independent traits in colonies: survival against bacterial challenge and maintenance of brood nest temperature. For both traits, we found hybrid and mixed colonies outperformed inbred colonies but did not perform differently from each other. During immune challenge assays, hybrid and mixed colonies experienced hazard ratios of 0.49 (95% CI [0.37, 0.65]) and 0.69 (95% CI [0.50, 0.96]) compared to inbred colonies. For nest temperatures, hybrid and mixed colonies experienced 1.94±0.97°C and 2.82±2.46°C less thermal error and 0.14±0.11°C2 and 0.16±0.06°C2 less thermal variance per hour than inbred lines. This suggests social and individual heterosis operate independently and may have similar effect sizes. These results highlight the importance of both inter- and intra-individual diversity to fitness, which may help explain the emergence of polyandry/polygyny in eusocial insects and inform breeding efforts in these systems.
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BACKGROUND: Venoms, which have evolved numerous times in animals, are ideal models of convergent trait evolution. However, detailed genomic studies of toxin-encoding genes exist for only a few animal groups. The hyper-diverse hymenopteran insects are the most speciose venomous clade, but investigation of the origin of their venom genes has been largely neglected. RESULTS: Utilizing a combination of genomic and proteo-transcriptomic data, we investigated the origin of 11 toxin genes in 29 published and 3 new hymenopteran genomes and compiled an up-to-date list of prevalent bee venom proteins. Observed patterns indicate that bee venom genes predominantly originate through single gene co-option with gene duplication contributing to subsequent diversification. CONCLUSIONS: Most Hymenoptera venom genes are shared by all members of the clade and only melittin and the new venom protein family anthophilin1 appear unique to the bee lineage. Most venom proteins thus predate the mega-radiation of hymenopterans and the evolution of the aculeate stinger.
Assuntos
Venenos de Abelha , Abelhas/genética , Animais , Perfilação da Expressão Gênica , Transcriptoma , Genômica , Duplicação GênicaRESUMO
Developmental plasticity generates phenotypic variation, but how it contributes to evolutionary change is unclear. Phenotypes of individuals in caste-based (eusocial) societies are particularly sensitive to developmental processes, and the evolutionary origins of eusociality may be rooted in developmental plasticity of ancestral forms. We used an integrative genomics approach to evaluate the relationships among developmental plasticity, molecular evolution, and social behavior in a bee species (Megalopta genalis) that expresses flexible sociality, and thus provides a window into the factors that may have been important at the evolutionary origins of eusociality. We find that differences in social behavior are derived from genes that also regulate sex differentiation and metamorphosis. Positive selection on social traits is influenced by the function of these genes in development. We further identify evidence that social polyphenisms may become encoded in the genome via genetic changes in regulatory regions, specifically in transcription factor binding sites. Taken together, our results provide evidence that developmental plasticity provides the substrate for evolutionary novelty and shapes the selective landscape for molecular evolution in a major evolutionary innovation: Eusociality.
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Abelhas/crescimento & desenvolvimento , Abelhas/fisiologia , Animais , Abelhas/genética , Comportamento Animal , Evolução Biológica , Evolução Molecular , Feminino , Genoma de Inseto , Proteínas de Insetos/genética , Proteínas de Insetos/metabolismo , Masculino , Metamorfose Biológica , Comportamento SocialRESUMO
While much of the focus of sociobiology concerns identifying genomic changes that influence social behaviour, we know little about the consequences of social behaviour on genome evolution. It has been hypothesized that social evolution can influence the strength of negative selection via two mechanisms. First, division of labour can influence the efficiency of negative selection in a caste-specific manner; indirect negative selection on worker traits is theoretically expected to be weaker than direct selection on queen traits. Second, increasing social complexity is expected to lead to relaxed negative selection because of its influence on effective population size. We tested these two hypotheses by estimating the strength of negative selection in honeybees, bumblebees, paper wasps, fire ants and six other insects that span the range of social complexity. We found no consistent evidence that negative selection was significantly stronger on queen-biased genes relative to worker-biased genes. However, we found strong evidence that increased social complexity reduced the efficiency of negative selection. Our study clearly illustrates how changes in behaviour can influence patterns of genome evolution by modulating the strength of natural selection.
Assuntos
Comportamento Animal , Evolução Biológica , Genoma de Inseto , Comportamento Social , Animais , Formigas/genética , Abelhas/genética , Insetos/genética , Fenótipo , Seleção Genética , VespasRESUMO
The Kinship Theory of Genomic Imprinting (KTGI) posits that, in species where females mate with multiple males, there is selection for a male to enhance the reproductive success of his offspring at the expense of other males and his mating partner. Reciprocal crosses between honey bee subspecies show parent-of-origin effects for reproductive traits, suggesting that males modify the expression of genes related to female function in their female offspring. This effect is likely to be greater in the Cape honey bee (Apis mellifera capensis), because a male's daughters have the unique ability to produce female offspring that can develop into reproductive workers or the next queen without mating. We generated reciprocal crosses between Capensis and another subspecies and used RNA-seq to identify transcripts that are over- or underexpressed in the embryos, depending on the parental origin of the gene. As predicted, 21 genes showed expression bias towards the Capensis father's allele in colonies with a Capensis father, with no such bias in the reciprocal cross. A further six genes showed a consistent bias towards expression of the father's allele across all eight colonies examined, regardless of the direction of the cross. Consistent with predictions of the KTGI, six of the 21 genes are associated with female reproduction. No gene consistently showed overexpression of the maternal allele.
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Impressão Genômica , Reprodução , Alelos , Animais , Abelhas/genética , Feminino , Expressão Gênica , Masculino , FenótipoRESUMO
Inbreeding (the mating between closely related individuals) often has detrimental effects that are associated with loss of heterozygosity at overdominant loci, and the expression of deleterious recessive alleles. However, determining which loci are detrimental when homozygous, and the extent of their phenotypic effects, remains poorly understood. Here, we utilize a unique inbred population of clonal (thelytokous) honey bees, Apis mellifera capensis, to determine which loci reduce individual fitness when homozygous. This asexual population arose from a single worker ancestor approximately 20 years ago and has persisted for at least 100 generations. Thelytokous parthenogenesis results in a 1/3 of loss of heterozygosity with each generation. Yet, this population retains heterozygosity throughout its genome due to selection against homozygotes. Deep sequencing of one bee from each of the three known sub-lineages of the population revealed that 3,766 of 10,884 genes (34%) have retained heterozygosity across all sub-lineages, suggesting that these genes have heterozygote advantage. The maintenance of heterozygosity in the same genes and genomic regions in all three sub-lineages suggests that nearly every chromosome carries genes that show sufficient heterozygote advantage to be selectively detrimental when homozygous.
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Abelhas/genética , Genoma de Inseto , Heterozigoto , Partenogênese , Seleção Genética , Animais , EndogamiaRESUMO
The Anthropocene is an epoch hallmarked by intensified human intrusion across ecosystems. One such intrusion is the movement and re-introduction of long-separated populations. By facilitating introgression - intraspecific genetic admixture - secondary contact can facilitate range expansion and the establishment of invasive species. The proximate mechanisms through which introgression facilitates expansion are rarely known (Bock et al., ; Rius & Darling, ), but managed species provide a useful avenue for exploration. Bee-keepers have been interbreeding highly diverged honeybee clades for centuries, often to introduce "useful" phenotypic variation to their stocks. Across the Western honeybee's (Apis mellifera) European range, this practice has not resulted in range expansion (Moritz, Härtel, & Neumann, ). In the Americas, however, introgression of European with African subspecies resulted in a widely publicized invasive population: The Africanized honeybee (AHB). In this issue of Molecular Ecology, Nelson, Wallberg, Simões, Lawson, and Webster () have made the first step towards understanding how this invasive species successfully spread across the Americas.
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Aclimatação , Adaptação Fisiológica , Alelos , Animais , Abelhas , Brasil , EcologiaRESUMO
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.
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Adaptação Biológica/genética , Abelhas/genética , Evolução Biológica , Variação Genética , Hierarquia Social , Metagenômica , Seleção Genética , Animais , Sequência de Bases , Dados de Sequência Molecular , Análise de Sequência de DNARESUMO
The honey bee is a key pollinator in agricultural operations as well as a model organism for studying the genetics and evolution of social behavior. The Apis mellifera genome has been sequenced and annotated twice over, enabling proteomics and functional genomics methods for probing relevant aspects of their biology. One troubling trend that emerged from proteomic analyses is that honey bee peptide samples consistently result in lower peptide identification rates compared with other organisms. This suggests that the genome annotation can be improved, or atypical biological processes are interfering with the mass spectrometry workflow. First, we tested whether high levels of polymorphisms could explain some of the missed identifications by searching spectra against the reference proteome (OGSv3.2) versus a customized proteome of a single honey bee, but our results indicate that this contribution was minor. Likewise, error-tolerant peptide searches lead us to eliminate unexpected post-translational modifications as a major factor in missed identifications. We then used a proteogenomic approach with ~1500 raw files to search for missing genes and new exons, to revive discarded annotations and to identify over 2000 new coding regions. These results will contribute to a more comprehensive genome annotation and facilitate continued research on this important insect.
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Abelhas/genética , Genoma de Inseto/genética , Genômica/métodos , Anotação de Sequência Molecular/métodos , Animais , Abelhas/metabolismo , Proteínas de Insetos/genética , Proteínas de Insetos/metabolismo , Espectrometria de Massas/métodos , Polimorfismo de Nucleotídeo Único , Processamento de Proteína Pós-Traducional , Proteólise , Proteoma/genética , Proteoma/metabolismo , Proteômica/métodosRESUMO
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.
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Abelhas/genética , Comportamento Animal , Evolução Molecular , Recombinação Genética , Animais , Abelhas/fisiologia , Dados de Sequência MolecularRESUMO
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 (â¼10.5 kb) and 20 randomly chosen genes (â¼16.5 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.
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Abelhas/genética , Evolução Molecular , Imunidade Inata/genética , Redes e Vias Metabólicas/genética , Proteínas/genética , Animais , Sequência de Bases , Abelhas/imunologia , Insetos/genética , Insetos/imunologia , Filogenia , Proteínas/imunologia , Comportamento SocialRESUMO
Nestmate recognition in ants is regulated through the detection of cuticular hydrocarbons by odorant receptors (ORs) in the antennae. These ORs are crucial for maintaining colony cohesion that allows invasive ant species to dominate colonized environments. In the invasive Argentine ant, Linepithema humile, ORs regulating nestmate recognition are thought to be present in a clade of nine-exon odorant receptors, but the identity of the specific genes remains unknown. We sought to narrow down the list of candidate genes using transcriptomics and phylostratigraphy. Comparative transcriptomic analyses were conducted on the antennae, head, thorax, and legs of Argentine ant workers. We have identified a set of twenty-one nine-exon odorant receptors enriched in the antennae compared to the other tissues, allowing for downstream verification of whether they can detect Argentine ant cuticular hydrocarbons. Further investigation of these ORs could allow us to further understand the mechanisms underlying nestmate recognition and colony cohesion in ants.
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Formigas , Filogenia , Receptores Odorantes , Animais , Formigas/genética , Formigas/metabolismo , Receptores Odorantes/genética , Receptores Odorantes/metabolismo , Transcriptoma , Perfilação da Expressão Gênica , Antenas de Artrópodes/metabolismo , Proteínas de Insetos/genética , Proteínas de Insetos/metabolismoRESUMO
The northern giant hornet Vespa mandarinia (NGH) is a voracious predator of other insect species, including honey bees. NGH's native range spans subtropical and temperate regions across much of east and southeast Asia and, in 2019, exotic populations of the species were discovered in North America. Despite this broad range and invasive potential, investigation of the population genomic structure of NGH across its native and introduced ranges has thus far been limited to a small number of mitochondrial samples. Here, we present analyses of genomic data from NGH individuals collected across the species' native range and from exotic individuals collected in North America. We provide the first survey of whole-genome population variation for any hornet species, covering this species' native and invasive ranges, and in doing so confirm likely origins in Japan and South Korea for the two introductions. We additionally show that, while this introduced population exhibited strongly elevated levels of inbreeding, these signatures of inbreeding are also present in some long-standing native populations, which may indicate that inbreeding depression alone is insufficient to prevent the persistence of NGH populations. As well as highlighting the importance of ongoing monitoring and eradication efforts to limit the spread of this species outside of its natural range, our data will serve as a foundational database for future genomic studies into introduced hornet populations.
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Espécies Introduzidas , Vespas , Animais , América do Norte , Vespas/genética , Genética Populacional , Genômica/métodos , Variação Genética , Endogamia , Genoma de InsetoRESUMO
De la Rúa et al. (2013) express some concerns about the conclusions of our recent study showing that management increases genetic diversity of honey bees (Apis mellifera) by promoting admixture (Harpur et al. 2012). We provide a brief review of the literature on the population genetics of A. mellifera and show that we utilized appropriate sampling methods to estimate genetic diversity in the focal populations. Our finding of higher genetic diversity in two managed A. mellifera populations on two different continents is expected to be the norm given the large number of studies documenting admixture in honey bees. Our study focused on elucidating how management affects genetic diversity in honey bees, not on how to best manage bee colonies. We do not endorse the intentional admixture of honey bee populations, and we agree with De la Rúa et al. (2013) that native honey bee subspecies should be conserved.
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Criação de Animais Domésticos , Abelhas/genética , Variação Genética , Genética Populacional , AnimaisRESUMO
Introduction: Social organisms, including honey bees (Apis mellifera L.), have defense mechanisms to control the multiplication and transmission of parasites and pathogens within their colonies. Self-grooming, a mechanism of behavioral immunity, seems to contribute to restrain the population growth of the ectoparasitic mite Varroa destructor in honey bee colonies. Because V. destructor is the most damaging parasite of honey bees, breeding them for resistance against the mite is a high priority of the beekeeping industry. Methods: A bidirectional breeding program to select honey bee colonies with low and high V. destructor population growth (LVG and HVG, respectively) was conducted. Having high and low lines of bees allowed the study of genetic mechanisms underlying self-grooming behavior between the extreme genotypes. Worker bees were classified into two categories: 'light groomers' and 'intense groomers'. The brains of bees from the different categories (LVG-intense, LVG-light, HVG-intense, and HVG-light) were used for gene expression and viral quantification analyses. Differentially expressed genes (DEGs) associated with the LVG and HVG lines were identified. Results: Four odorant-binding proteins and a gustatory receptor were identified as differentially expressed genes. A functional enrichment analysis showed 19 enriched pathways from a list of 219 down-regulated DEGs in HVG bees, including the Kyoto Encyclopedia of Genes and Genomes (KEGG) term of oxidative phosphorylation. Additionally, bees from the LVG line showed lower levels of Apis rhabdovirus 1 and 2, Varroa destructor virus -1 (VDV-1/DWV-B), and Deformed wing virus-A (DWV-A) compared to bees of the HVG line. The difference in expression of odorant-binding protein genes and a gustatory receptor between bee lines suggests a possible link between them and the perception of irritants to trigger rapid self-grooming instances that require the activation of energy metabolic pathways. Discussion: These results provide new insights on the molecular mechanisms involved in honey bee grooming behavior. Differences in viral levels in the brains of LVG and HVG bees showed the importance of investigating the pathogenicity and potential impacts of neurotropic viruses on behavioral immunity. The results of this study advance the understanding of a trait used for selective breeding, self-grooming, and the potential of using genomic assisted selection to improve breeding programs.
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Social insects are very successful invasive species, and the continued increase of global trade and transportation has exacerbated this problem. The yellow-legged hornet, Vespa velutina nigrithorax (henceforth Asian hornet), is drastically expanding its range in Western Europe. As an apex insect predator, this hornet poses a serious threat to the honey bee industry and endemic pollinators. Current suppression methods have proven too inefficient and expensive to limit its spread. Gene drives might be an effective tool to control this species, but their use has not yet been thoroughly investigated in social insects. Here, we built a model that matches the hornet's life history and modelled the effect of different gene drive scenarios on an established invasive population. To test the broader applicability and sensitivity of the model, we also incorporated the invasive European paper wasp Polistes dominula. We find that, due to the haplodiploidy of social hymenopterans, only a gene drive targeting female fertility is promising for population control. Our results show that although a gene drive can suppress a social wasp population, it can only do so under fairly stringent gene drive-specific conditions. This is due to a combination of two factors: first, the large number of surviving offspring that social wasp colonies produce make it possible that, even with very limited formation of resistance alleles, such alleles can quickly spread and rescue the population. Second, due to social wasp life history, infertile individuals do not compete with fertile ones, allowing fertile individuals to maintain a large population size even when drive alleles are widespread. Nevertheless, continued improvements in gene drive technology may make it a promising method for the control of invasive social insects in the future.
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Tecnologia de Impulso Genético , Vespas , Feminino , Abelhas/genética , Animais , Vespas/genética , Europa (Continente) , Fertilidade , Espécies IntroduzidasRESUMO
Nucleic acid sensing powered by the sequence recognition of CRIPSR technologies has enabled major advancement toward rapid, accurate and deployable diagnostics. While exciting, there are still many challenges facing their practical implementation, such as the widespread need for a PAM sequence in the targeted nucleic acid, labile RNA inputs, and limited multiplexing. Here we report FACT (Functionalized Amplification CRISPR Tracing), a CRISPR-based nucleic acid barcoding technology compatible with Cas12a and Cas13a, enabling diagnostic outputs based on cis- and trans-cleavage from any sequence. Furthermore, we link the activation of CRISPR-Cas12a to the expression of proteins through a Reprogrammable PAIRing system (RePAIR). We then combine FACT and RePAIR to create FACTOR (FACT on RePAIR), a CRISPR-based diagnostic, that we use to detect infectious disease in an agricultural use case: honey bee viral infection. With high specificity and accuracy, we demonstrate the potential of FACTOR to be applied to the sensing of any nucleic acid of interest.
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Técnicas Biossensoriais , Ácidos Nucleicos , Animais , DNA/genética , Agricultura , Cabeça , RNA/genética , Sistemas CRISPR-Cas/genética , Técnicas de Amplificação de Ácido NucleicoRESUMO
The extreme conservation of mitochondrial genomes in metazoans poses a significant challenge to understanding mitogenome evolution. However, the presence of variation in gene order or genome structure, found in a small number of taxa, can provide unique insights into this evolution. Previous work on two stingless bees in the genus Tetragonula (T. carbonaria and T. hockingsi) revealed highly divergent CO1 regions between them and when compared to the bees from the same tribe (Meliponini), indicating rapid evolution. Using mtDNA isolation and Illumina sequencing, we elucidated the mitogenomes of both species. In both species, there has been a duplication of the whole mitogenome to give a total genome size of 30,666 bp in T. carbonaria; and 30,662 bp in T. hockingsi. These duplicated genomes present a circular structure with two identical and mirrored copies of all 13 protein coding genes and 22 tRNAs, with the exception of a few tRNAs that are present as single copies. In addition, the mitogenomes are characterized by rearrangements of two block of genes. We believe that rapid evolution is present in the whole Indo-Malay/Australasian group of Meliponini but is extraordinarily elevated in T. carbonaria and T. hockingsi, probably due to founder effect, low effective population size and the mitogenome duplication. All these features - rapid evolution, rearrangements, and duplication - deviate significantly from the vast majority of the mitogenomes described so far, making the mitogenomes of Tetragonula unique opportunities to address fundamental questions of mitogenome function and evolution.
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Abelhas , Genoma Mitocondrial , Animais , Austrália , Abelhas/genética , Genoma Mitocondrial/genética , Mitocôndrias/genética , FilogeniaRESUMO
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.
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Criação de Animais Domésticos , Abelhas/genética , Variação Genética , Genética Populacional , África , Animais , Teorema de Bayes , Cruzamento , Núcleo Celular/genética , Europa (Continente) , Técnicas de Genotipagem , Dados de Sequência Molecular , América do Norte , Análise de Sequência de DNARESUMO
Many species have separate haploid and diploid phases. Theory predicts that each phase should experience the effects of evolutionary forces (like selection) differently. In the haploid phase, all fitness-affecting alleles are exposed to selection, whereas in the diploid phase, those same alleles can be masked by homologous alleles. This predicts that selection acting on genes expressed in haploids should be more effective than diploid-biased genes. Unfortunately, in arrhenotokous species, this prediction can be confounded with the effects of sex-specific expression, as haploids are usually reproductive males. Theory posits that, when accounting for ploidal- and sex-specific expression, selection should be equally efficient on haploid- and diploid-biased genes relative to constitutive genes. Here, we used a multiomic approach in honey bees to quantify the evolutionary rates of haploid-biased genes and test the relative effects of sexual- and haploid-expression on molecular evolution. We found that 16% of the honey bee's protein-coding genome is highly expressed in haploid tissue. When accounting for ploidy and sex, haploid- and diploid-biased genes evolve at a lower rate than expected, indicating that they experience strong negative selection. However, the rate of molecular evolution of haploid-biased genes was higher than diploid-based genes. Genes associated with sperm storage are a clear exception to this trend with evidence of strong positive selection. Our results provide an important empirical test of theory outlining how selection acts on genes expressed in arrhenotokous species. We propose the haploid life history stage affects genome-wide patterns of diversity and divergence because of both sexual and haploid selection.