The draft genome of a socially polymorphic halictid bee,Lasioglossum albipes

Background

Taxa that harbor natural phenotypic variation are ideal for ecological genomic approaches aimed at understanding how the interplay between genetic and environmental factors can lead to the evolution of complex traits. Lasioglossum albipes is a polymorphic halictid bee that expresses variation in social behavior among populations, and common-garden experiments have suggested that this variation is likely to have a genetic component.

Results

We present the L. albipes genome assembly to characterize the genetic and ecological factors associated with the evolution of social behavior. The de novo assembly is comparable to other published social insect genomes, with an N50 scaffold length of 602 kb. Gene families unique to L. albipes are associated with integrin-mediated signaling and DNA-binding domains, and several appear to be expanded in this species, including the glutathione-s-transferases and the inositol monophosphatases. L. albipes has an intact DNA methylation system, and in silico analyses suggest that methylation occurs primarily in exons. Comparisons to other insect genomes indicate that genes associated with metabolism and nucleotide binding undergo accelerated evolution in the halictid lineage. Whole-genome resequencing data from one solitary and one social L. albipes female identify six genes that appear to be rapidly diverging between social forms, including a putative odorant receptor and a cuticular protein.

Conclusions

L. albipes represents a novel genetic model system for understanding the evolution of social behavior. It represents the first published genome sequence of a primitively social insect, thereby facilitating comparative genomic studies across the Hymenoptera as a whole.     

The influence of soil temperature on the nesting cycle of the halictid bee Lasioglossum malachurum

The physiology and behavior of ectothermic organisms is strongly influenced by temperature. For ground nesting species like the primitively eusocial halictid bee, Lasioglossum malachurum, soil temperature might influence the life cycle as well as the complexity of the social group since the number of broods that can be fitted into the flight season might increase with increasing temperature. Our study populationof L. malachurum at Wuerzburg exhibits a remarkable variability with respect to the number of broods and the pattern of sexual production. Broods are separated by activity pauses during which the larvae develop. In this study we investigate the influence of soil temperature on the pattern of nesting activity (duration of broods and pauses) and on the number of broods in L. malachurum. We observed a total of 1138 nests in 13 aggregations near Wuerzburg. As expected, soil temperature shortened the duration of the pauses, resulting in an overall shortening of the nesting cycle. This is most probably due to a physiological effect of soil temperature on the development of the larvae. With regard to the nesting strategies, we hypothesized that a shortening of the nesting cycle within the limited flight season should enhance the success of a strategy with more worker broods. In fact, patches with higher soil temperature showed more broods. However, this effect was rather weak, suggesting that other factors might have a stronger impact on the variability in nesting strategy within our study population of L. malachurum. Received 20 December 2005; revised 25 April 2006; accepted 2 May 2006. An erratum to this article is available at .     

Genetic differentiation across the social transition in a socially polymorphic sweat bee,Halictus rubicundus

Eusociality is widely considered a major evolutionary transition. The socially polymorphic sweat bee Halictus rubicundus, solitary in cooler regions of its Holarctic range and eusocial in warmer parts, is an excellent model organism to address this transition, and specifically the question of whether sociality is associated with a strong barrier to gene flow between phenotypically divergent populations. Mitochondrial DNA (COI) from specimens collected across the British Isles, where both solitary and social phenotypes are represented, displayed limited variation, but placed all specimens in the same European lineage; haplotype network analysis failed to differentiate solitary and social lineages. Microsatellite genetic variability was high and enabled us to quantify genetic differentiation among populations and social phenotypes across Great Britain and Ireland. Results from conceptually different analyses consistently showed greater genetic differentiation between geographically distant populations, independently of their social phenotype, suggesting that the two social forms are not reproductively isolated. A landscape genetic approach revealed significant isolation by distance (Mantel test r = 0.622, P < 0.001). The Irish Sea acts as physical barrier to gene flow (partial Mantel test r = 0.453, P < 0.01), indicating that geography, rather than expression of solitary or social behaviour (partial Mantel test r = −0.238, P = 0.053), had a significant effect on the genetic structure of H. rubicundus across the British Isles. Although we cannot reject the hypothesis of a genetic underpinning to differences in solitary and eusocial phenotypes, our data clearly demonstrate a lack of reproductive isolation between the two social forms.     

Shared reproduction and sex ratio adjustment to clutch size in a socially polymorphic orchid bee

Nests of the primitively eusocial orchid bee Euglossa viridissima are generally founded by a solitary female but can be reactivated by female offspring, in the presence or absence of the mother. The population therefore exists of solitary and social nests that co-occur in an area. A female can stay as a subordinate helper under a dominant female or disperse to become a solitary foundress. Yet, the costs and benefits of the different social phenotypes are so far little understood. Here, we compared solitary and social nests of orchid bees. We used offspring of solitary and social nests to calculate offspring sex ratio, and applied molecular markers to calculate intranidal relatedness, infer maternity and test whether sociality may have a genetic component. We found that social nests had on average more brood than solitary nests. The overall sex ratio in the population did not differ from 1:1. However, social nests tended to produce a split sex ratio with some nests producing mainly males and others mainly female offspring. Regardless of social phenotype, the number of offspring was correlated with the sex ratio, with smaller nests having a more female-biased offspring. In social nests, not all offspring resulted from a single-mated mother, which was also the case for some solitary nests. This suggests shared reproduction in social nests and may be an indication that intraspecific parasitism and nest takeover are not uncommon. Structure analyses did not reveal different genetic background of the two social phenotypes. Our results suggest that there is no clear benefit that favours one of the two social phenotypes over the other and that the population is kept at balance in terms of sex ratio.     

Phylogeography of the socially polymorphic sweat bee Halictus rubicundus (Hymenoptera: Halictidae)

The evolution of sociality in insects holds a central place in evolutionary theory. By examining the phylogenetic patterns of solitary and social behavior and how they correlate with ecological variables, we may identify factors important in the evolution of sociality. In this study, we investigated historical and biogeographical patterns of sociality in a socially polymorphic bee species (one that demonstrates both social and solitary nesting behavior). This unique system allows for a more powerful examination of evolutionary transitions in sociality than interspecific studies of obligately social and solitary species. We conducted a phylogenetic analysis among populations of the halictine bee Halictus rubicundus and then identified relationships among mitochondrial DNA sequence data, sociality, environmental conditions at the nesting site, and geographic location of populations of this species. Within North America, populations of H. rubicundus expressing social and solitary behavior belong to different genetic lineages. Sociality is also correlated with at least one environmental variable used in this study. Taken together, the results support the predictions for genetic control of sociality, but they are still consistent with social behavior at some level being determined by the environmental conditions at the nesting site.     

The determinants of queen size in a socially polymorphic ant

In social animals, body size can be shaped by multiple factors, such as direct genetic effects, maternal effects, or the social environment. In ants, the body size of queens correlates with the social structure of the colony: colonies headed by a single queen (monogyne) generally produce larger queens that are able to found colonies independently, whereas colonies headed by multiple queens (polygyne) tend to produce smaller queens that stay in their natal colony or disperse with workers. We performed a cross‐fostering experiment to investigate the proximate causes of queen size variation in the socially polymorphic ant Formica selysi. As expected if genetic or maternal effects influence queen size, eggs originating from monogyne colonies developed into larger queens than eggs collected from polygyne colonies, be they raised by monogyne or polygyne workers. In contrast, eggs sampled in monogyne colonies were smaller than eggs sampled in polygyne colonies. Hence, eggs from monogyne colonies are smaller but develop into larger queens than eggs from polygyne colonies, independently of the social structure of the workers caring for the brood. These results demonstrate that a genetic polymorphism or maternal effect transmitted to the eggs influences queen size, which probably affects the social structure of new colonies.     

Advantages and disadvantages of large colony size in a halictid bee: the queen's perspective

The size of the group of social species might influence basicaspects of productivity and social interactions. In many primitivelysocial insects, foundress queens are basically in control ofthe number of workers in their first brood. We examined factorsthat might influence the optimal number of workers a queen shouldproduce during the solitary founding phase in Lasioglossum malachurum(Hymenoptera, Halictidae). A priori, it seems plausible thatshe should produce as many workers as possible (1) to maximizecolony productivity and (2) to minimize the impact of broodparasitoids. However, there might also be unfavorable consequencesof a large colony size from the queen's perspective. First,the queen might incur disproportionately high costs that decreaseher potential for subsequent reproduction. Second, the queenmight not be able to suppress the development of ovaries ina large number of workers. As a clear advantage of a large colonysize, we found an increased production of sexuals. Contraryto our expectation, in the first worker phase, nests that wereparasitized by Sphecodes bees had more workers than did unparasitizednests. We found no evidence that the production of the firstworker brood entailed costs to the queen. However, the degreeof development of worker ovaries increased with colony size,and some degree of development was detectable with as few asfour workers. This study shows that the number of workers aqueen produces might depend on the interaction of several factors,some of which have not been considered in detail yet.     

The population genetics of a solitary oligolectic sweat bee, Lasioglossum (Sphecodogastra) oenotherae (Hymenoptera: Halictidae)

Strong evidence exists for global declines in pollinator populations. Data on the population genetics of solitary bees, especially diet specialists, are generally lacking. We studied the population genetics of the oligolectic bee Lasioglossum oenotherae, a specialist on the pollen of evening primrose (Onagraceae), by genotyping 455 females from 15 populations across the bee's North American range at six hyper-variable microsatellite loci. We found significant levels of genetic differentiation between populations, even at small geographic scales, as well as significant patterns of isolation by distance. However, using multilocus genotype assignment tests, we detected 11 first-generation migrants indicating that L. oenotherae's sub-populations are experiencing ongoing gene flow. Southern populations of L. oenotherae were significantly more likely to deviate from Hardy-Weinberg equilibrium and from genotypic equilibrium, suggesting regional differences in gene flow and/or drift and inbreeding. Short-term N(e) estimated using temporal changes in allele frequencies in several populations ranged from approximately 223 to 960. We discuss our findings in terms of the conservation genetics of specialist pollinators, a group of considerable ecological importance.     

蜜蜂全基因组出笼前后

在2006年10月26日,期待已久的蜜蜂的基因组序列在英国杂志《自然》上发表了。这一事件对于全世界蜜蜂生物学家来说,标志着蜜蜂研究“后基因组时代”的开始。这一重大项目由倍乐医学院完成,耗资800万美元,历时2年。而实际上对于基因组的注释又经过近2年的时间,由代表15个国家、来自64个实验室的170名科学家完成。这一等待是值得的基因组序列最终发表后,生物学家通过互联网能做他们自己的“数据采掘”,用这一可得的公共资源验证自己的假说。事实上,在蜜蜂基因组文章在《自然》上发表的当周,其姊妹刊上发表的约50篇相关论文中,有一半以上是基于生物信息学的研究,这些刊物包括《科学》、《基因组研究》、《美国国家科学院院报》及《昆虫分子生物学》。蜜蜂与人类享有一些共性劳动分工,复杂的通信系统包括语言,发达的保卫和防御系统,精妙的建筑以及为了共同利益自我牺牲的特点。由于有这些共性,蜜蜂基因组的发表将使科学家不仅能够深入研究蜜蜂生物学,而且能深入了解我们人类自身的生物学。     

Complex sociogenetic organization and the origin of unrelated workers in a eusocial sweat bee, Lasioglossum malachurum

Sweat bees (Halictidae) exhibit great interspecific and intraspecific diversity in their social organisation, yet there is remarkably little information on the sociogenetic organisation of any species. Lasioglossum malachurum is a eusocial sweat bee with an annual lifecycle that exhibits considerable variation in its social organisation across its wide geographic range from northern to southern Europe. We collected all adults from 31 L. malachurum nests at Eichkogl, Austria, near the latitudinal centre of its distribution, and genotyped 148 workers using 5 highly variable microsatellite loci developed for this species. Nests were often queenless (48% of nests) during the second phase of worker activity, when colonies were provisioning the sexual brood. Pedigree reconstruction and estimates of nestmate genetic relatedness demonstrated that nests often (32% of nests) contained alien workers, probably as a result of worker drifting from their natal to a foreign nest. Queen effective mating frequency was variable (harmonic mean m_e = 1.24), but sometimes high (maximum 2.7). These data demonstrate that nests of L. malachurum do not have a classical eusocial sociogenetic organisation (monogyny, monandry) and thereby pose a challenge to exclusively relatedness based arguments for the evolution of eusociality in the taxon. Received 6 June 2008; revised 1 October 2008; accepted 13 October 2008.     

Discovery of wood nesting by a subterranean halictine bee,Lasioglossum (Evylaeus) vulsum (Hymenoptera: Halictidae)

An unusual nesting substrate of a subterranean halictine bee, Lasioglossum (Evylaeus) vulsum (Vachal), was found at Mt Ishizuchi‐san, Ehime, Japan. Two nests were obtained from a decaying log in a display sign for a local restaurant. Brood cells, forming a cell cluster, were constructed in a wood hollow with rotted wood fibers pressed together. Nests in the decaying log show the same structural elements as those made in soil. This is the first report of wood nesting by subterranean halictine bees belonging to the subgenus Evylaeus.     

Lasiocepsin, a novel cyclic antimicrobial peptide from the venom of eusocial bee Lasioglossum laticeps (Hymenoptera: Halictidae)

In the venom of eusocial bee Lasioglossum laticeps, we identified a novel unique antimicrobial peptide named lasiocepsin consisting of 27 amino acid residues and two disulfide bridges. After identifying its primary structure, we synthesized lasiocepsin by solid-phase peptide synthesis using two different approaches for oxidative folding. The oxidative folding of fully deprotected linear peptide resulted in a mixture of three products differing in the pattern of disulfide bridges. Regioselective disulfide bond formation significantly improved the yield of desired product. The synthetic lasiocepsin possessed antimicrobial activity against both Gram-positive and -negative bacteria, antifungal activity against Candida albicans, and no hemolytic activity against human erythrocytes. We synthesized two lasiocepsin analogs cyclized through one native disulfide bridge in different positions and having the remaining two cysteines substituted by alanines. The analog cyclized through a Cys8-Cys25 disulfide bridge showed reduced antimicrobial activity compared to the native peptide while the second one (Cys17-Cys27) was almost inactive. Linear lasiocepsin having all four cysteine residues substituted by alanines or alkylated was also inactive. That was in contrast to the linear lasiocepsin with all four cysteine residues non-paired, which exhibited remarkable antimicrobial activity. The shortening of lasiocepsin by several amino acid residues either from the N- or C-terminal resulted in significant loss of antimicrobial activity. Study of Bacillus subtilis cells treated by lasiocepsin using transmission electron microscopy showed leakage of bacterial content mainly from the holes localized at the ends of the bacterial cells.     

The first draft of the pigeonpea genome sequence

Pigeonpea (Cajanus cajan) is an important grain legume of the Indian subcontinent, South-East Asia and East Africa. More than eighty five percent of the world pigeonpea is produced and consumed in India where it is a key crop for food and nutritional security of the people. Here we present the first draft of the genome sequence of a popular pigeonpea variety ??Asha??. The genome was assembled using long sequence reads of 454 GS-FLX sequencing chemistry with mean read lengths of >550?bp and >10-fold genome coverage, resulting in 510,809,477?bp of high quality sequence. Total 47,004 protein coding genes and 12,511 transposable elements related genes were predicted. We identified 1,213 disease resistance/defense response genes and 152 abiotic stress tolerance genes in the pigeonpea genome that make it a hardy crop. In comparison to soybean, pigeonpea has relatively fewer number of genes for lipid biosynthesis and larger number of genes for cellulose synthesis. The sequence contigs were arranged in to 59,681 scaffolds, which were anchored to eleven chromosomes of pigeonpea with 347 genic-SNP markers of an intra-species reference genetic map. Eleven pigeonpea chromosomes showed low but significant synteny with the twenty chromosomes of soybean. The genome sequence was used to identify large number of hypervariable ??Arhar?? simple sequence repeat (HASSR) markers, 437 of which were experimentally validated for PCR amplification and high rate of polymorphism among pigeonpea varieties. These markers will be useful for fingerprinting and diversity analysis of pigeonpea germplasm and molecular breeding applications. This is the first plant genome sequence completed entirely through a network of Indian institutions led by the Indian Council of Agricultural Research and provides a valuable resource for the pigeonpea variety improvement.     

Complex sociogenetic organization and reproductive skew in a primitively eusocial sweat bee,Lasioglossum malachurum,as revealed by microsatellites

The sweat bees (Family Halictidae) are a socially diverse taxon in which eusociality has arisen independently numerous times. The obligate, primitively eusocial Lasioglossum malachurum, distributed widely throughout Europe, has been considered the zenith of sociality within halictids. A single queen heads a colony of smaller daughter workers which, by mid-summer, produce new sexuals (males and gynes), of which only the mated gynes overwinter to found new colonies the following spring. We excavated successfully 18 nests during the worker- and gyne-producing phases of the colony cycle and analysed each nest's queen and either all workers or all gynes using highly variable microsatellite loci developed specifically for this species. Three important points arise from our analyses. First, queens are facultatively polyandrous (queen effective mating frequency: range 1-3, harmonic mean 1.13). Second, queens may head colonies containing unrelated individuals (n = 6 of 18 nests), most probably a consequence of colony usurpation during the early phase of the colony cycle before worker emergence. Third, nonqueen's workers may, but the queen's own workers do not, lay fertilized eggs in the presence of the queen that successfully develop into gynes, in agreement with so-called 'concession' models of reproductive skew.     

Lasioglossum (Dialictus) tenax (Sandhouse) (Hymenoptera: Halictidae) as a solitary sweat bee

Summary Nine nests ofLasioglossum (Dialictus) tenax were excavated near Calgary, Alberta, Canada over a time period encompassing the entire brood production period in 1988. Each nest contained a maximum of one active adult female, nest productivity peaked in mid July, protandry was noted and no significant size difference between foundresses and the earlier emerging females was detected. These data suggest that this species is solitary. These results are compared with data for the sympatrically nesting eusocial speciesL. (D.) laevissimum.