Kocher SD, Li C, Yang W, Tan H, Yi SV, Yang XY, Hoekstra HE, Zhang GJ, Pierce NE, Yu DW.
The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes. Genome Biology. 2013;14.
AbstractBackground: 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.
Talavera G, Lukhtanov VA, Rieppel L, Pierce NE, Vila R.
In the shadow of phylogenetic uncertainty: The recent diversification of Lysandra butterflies through chromosomal change. Molecular Phylogenetics and Evolution. 2013;69 :469-478.
AbstractThe phylogeny of the butterfly genus Lysandra (Lycaenidae, Polyommatinae) has been intractable using both molecular and morphological characters, which could be a result of speciation due to karyotype instability. Here we reconstruct the phylogeny of the group using multi-locus coalescent-based methods on seven independent genetic markers. While the genus is ca. 4.9 Mya old, the diversification of the extant lineages was extremely recent (ca. 1.5 Mya) and involved multiple chromosomal rearrangements. We find that relationships are uncertain due to both incomplete lineage sorting and hybridization. Minimizing the impact of reticulation in inferring the species tree by testing for mitochondria] introgression events yields a partially resolved tree with three main supported clades: L. punctifera + L. bellargus, the corydonius taxa, and L coridon + the Iberian taxa, plus three independent lineages without apparently close relatives (L. ossmar, L syriaca and L. dezina). Based on these results and new karyotypic data, we propose a rearrangement recognizing ten species within the genus. Finally, we hypothesize that chromosomal instability may have played a crucial role in the Lysandra recent diversification. New chromosome rearrangements might be fixed in populations after severe bottlenecks, which at the same time might promote rapid sorting of neutral molecular markers. We argue that population bottlenecks might be a prerequisite for chromosomal speciation in this group. (C) 2013 Elsevier Inc. All rights reserved.
Kronauer DJC, Tsuji K, Pierce NE, Keller L.
Non-nest mate discrimination and clonal colony structure in the parthenogenetic ant Cerapachys biroi. Behavioral Ecology. 2013;24 :617-622.
AbstractUnderstanding the interplay between cooperation and conflict in social groups is a major goal of biology. One important factor is genetic relatedness, and animal societies are usually composed of related but genetically different individuals, setting the stage for conflicts over reproductive allocation. Recently, however, it has been found that several ant species reproduce predominantly asexually. Although this can potentially give rise to clonal societies, in the few well-studied cases, colonies are often chimeric assemblies of different genotypes, due to worker drifting or colony fusion. In the ant Cerapachys biroi, queens are absent and all individuals reproduce via thelytokous parthenogenesis, making this species an ideal study system of asexual reproduction and its consequences for social dynamics. Here, we show that colonies in our study population on Okinawa, Japan, recognize and effectively discriminate against foreign workers, especially those from unrelated asexual lineages. In accord with this finding, colonies never contained more than a single asexual lineage and average pairwise genetic relatedness within colonies was extremely high (r = 0.99). This implies that the scope for social conflict in C. biroi is limited, with unusually high potential for cooperation and altruism.
Groen SC, Whiteman NK, Bahrami AK, Wilczek AM, Cui JP, Russell JA, Cibrian-Jaramillo A, Butler IA, Rana JD, Huang GH, et al. Pathogen-Triggered Ethylene Signaling Mediates Systemic-Induced Susceptibility to Herbivory in Arabidopsis. Plant Cell. 2013;25 :4755-4766.
AbstractMulticellular eukaryotic organisms are attacked by numerous parasites from diverse phyla, often simultaneously or sequentially. An outstanding question in these interactions is how hosts integrate signals induced by the attack of different parasites. We used a model system comprised of the plant host Arabidopsis thaliana, the hemibiotrophic bacterial phytopathogen Pseudomonas syringae, and herbivorous larvae of the moth Trichoplusia ni (cabbage looper) to characterize mechanisms involved in systemic-induced susceptibility (SIS) to T. ni herbivory caused by prior infection by virulent P. syringae. We uncovered a complex multilayered induction mechanism for SIS to herbivory. In this mechanism, antiherbivore defenses that depend on signaling via (1) the jasmonic acid-isoleucine conjugate (JA-Ile) and (2) other octadecanoids are suppressed by microbe-associated molecular pattern-triggered salicylic acid (SA) signaling and infection-triggered ethylene signaling, respectively. SIS to herbivory is, in turn, counteracted by a combination of the bacterial JA-Ile mimic coronatine and type III virulence-associated effectors. Our results show that SIS to herbivory involves more than antagonistic signaling between SA and JA-Ile and provide insight into the unexpectedly complex mechanisms behind a seemingly simple trade-off in plant defense against multiple enemies.
McFall-Ngai M, Hadfield MG, Bosch TCG, Carey HV, Domazet-Loso T, Douglas AE, Dubilier N, Eberl G, Fukami T, Gilbert SF, et al. Animals in a bacterial world, a new imperative for the life sciences. Proceedings of the National Academy of Sciences of the United States of America. 2013;110 :3229-3236.
AbstractIn the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal-bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other's genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal-bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.
2013_mcfall-ngai_et_al_animals_in_a_bacterial_world.pdf Martins DJ, Collins SC, Congdon C, Pierce NE.
Association between the African lycaenid, Anthene usamba, and an obligate acacia ant, Crematogaster mimosae. Biological Journal of the Linnean Society. 2013;109 :302-312.
AbstractThe African lycaenid butterfly, Anthene usamba, is an obligate myrmecophile of the acacia ant, Crematogaster mimosae. Female butterflies use the presence of C.mimosae as an oviposition cue. The eggs are laid on the foliage and young branches of the host plant, Acacia drepanolobium. Larvae shelter in the swollen thorns (domatia) of the host tree, where they live in close association with the acacia ants, and each larva occupies a domatium singly. Anthene usamba are tended by ants that feed from the dorsal nectary organ at regular intervals. Larvae also possess tentacle organs flanking the dorsal nectary organ and appear to signal to ants by everting these structures. Larvae were observed to spend most of their time within the domatia. Stable isotope analysis of matched host plantantbutterfly samples revealed that Anthene usamba are 15N enriched relative to the ants with which they associate. These data, based on the increase in 15N through trophic levels, indicate that the caterpillars of these butterflies are aphytophagous and either exploit the ant brood of C.mimosae within the domatia, or are fed mouth to mouth by adult workers via trophallaxis. This is the first documented case of aphytophagy in African Anthene. Pupation occurs inside the domatium and the imago emerges and departs via the hole chewed by the larva. The adult females remain closely associated with their natal patch of trees, whereas males disperse more widely across the acacia savannah. Females prefer to oviposit on trees with the specific host ant, C.mimosae, an aggressive obligate mutualist, and avoid neighbouring trees with other ant species. Adult butterflies are active during most months of the year, and there are at least two to three generations each year. Observations made over a 5-year period indicate that a number of different lycaenid species utilize ant-acacias in East Africa, and these observations are summarized, together with comparisons from the literature.(c) 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109, 302312.
2013_martins_et_al_anthene.pdf Basset Y, Eastwood R, Sam L, Lohman DJ, Novotny V, Treuer T, Miller SE, Weiblen GD, Pierce NE, Bunyavejchewin S, et al. Cross-continental comparisons of butterfly assemblages in tropical rainforests: implications for biological monitoring. Insect Conservation and Diversity. 2013;6 :223-233.
Abstract. 1.Standardised transect counts of butterflies in old-growth rainforests in different biogeographical regions are lacking. Such data are needed to mitigate the influence of methodological and environmental factors within and between sites and, ultimately, to discriminate between long-term trends and short-term stochastic changes in abundance and community composition. 2.We compared butterfly assemblages using standardised Pollard Walks in the understory of closed-canopy lowland tropical rainforests across three biogeographical regions: Barro Colorado Island (BCI), Panama; Khao Chong (KHC), Thailand; and Wanang (WAN), Papua New Guinea. 3.The length and duration of transects, their spatial autocorrelation, and number of surveys per year represented important methodological factors that strongly influenced estimates of butterfly abundance. Of these, the effect of spatial autocorrelation was most difficult to mitigate across study sites. 4.Butterfly abundance and faunal composition were best explained by air temperature, elevation, rainfall, wind velocity, and human disturbance at BCI and KHC. In the absence of weather data at WAN, duration of transects and number of forest gaps accounted for most of the explained variance, which was rather low in all cases (<33%). 5.Adequate monitoring of the abundance of common butterflies was achieved at the 50ha BCI plot, with three observers walking each of 10 transects of 500m for 30min each, during each of four surveys per year. These data may be standardised further after removing outliers of temperature and rainfall. Practical procedures are suggested to implement global monitoring of rainforest butterflies with Pollard Walks.
cross_continent.pdf Kocher SD, Li C, Yang W, Tan H, Yi SV, Yang XY, Hoekstra HE, Zhang GJ, Pierce NE, Yu DW.
The draft genome of a socially polymorphic halictid bee, Lasioglossum albipes. Genome Biology. 2013;14.
AbstractBackground: 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.
2013_kocher_et_al.pdf Talavera G, Lukhtanov VA, Rieppel L, Pierce NE, Vila R.
In the shadow of phylogenetic uncertainty: The recent diversification of Lysandra butterflies through chromosomal change. Molecular Phylogenetics and Evolution. 2013;69 :469-478.
AbstractThe phylogeny of the butterfly genus Lysandra (Lycaenidae, Polyommatinae) has been intractable using both molecular and morphological characters, which could be a result of speciation due to karyotype instability. Here we reconstruct the phylogeny of the group using multi-locus coalescent-based methods on seven independent genetic markers. While the genus is ca. 4.9 Mya old, the diversification of the extant lineages was extremely recent (ca. 1.5 Mya) and involved multiple chromosomal rearrangements. We find that relationships are uncertain due to both incomplete lineage sorting and hybridization. Minimizing the impact of reticulation in inferring the species tree by testing for mitochondria] introgression events yields a partially resolved tree with three main supported clades: L. punctifera + L. bellargus, the corydonius taxa, and L coridon + the Iberian taxa, plus three independent lineages without apparently close relatives (L. ossmar, L syriaca and L. dezina). Based on these results and new karyotypic data, we propose a rearrangement recognizing ten species within the genus. Finally, we hypothesize that chromosomal instability may have played a crucial role in the Lysandra recent diversification. New chromosome rearrangements might be fixed in populations after severe bottlenecks, which at the same time might promote rapid sorting of neutral molecular markers. We argue that population bottlenecks might be a prerequisite for chromosomal speciation in this group. (C) 2013 Elsevier Inc. All rights reserved.
2013_talavera_et_al.pdf 2013_talavera_et_al_supplement.pdf Kronauer DJC, Tsuji K, Pierce NE, Keller L.
Non-nest mate discrimination and clonal colony structure in the parthenogenetic ant Cerapachys biroi. Behavioral Ecology. 2013;24 :617-622.
AbstractUnderstanding the interplay between cooperation and conflict in social groups is a major goal of biology. One important factor is genetic relatedness, and animal societies are usually composed of related but genetically different individuals, setting the stage for conflicts over reproductive allocation. Recently, however, it has been found that several ant species reproduce predominantly asexually. Although this can potentially give rise to clonal societies, in the few well-studied cases, colonies are often chimeric assemblies of different genotypes, due to worker drifting or colony fusion. In the ant Cerapachys biroi, queens are absent and all individuals reproduce via thelytokous parthenogenesis, making this species an ideal study system of asexual reproduction and its consequences for social dynamics. Here, we show that colonies in our study population on Okinawa, Japan, recognize and effectively discriminate against foreign workers, especially those from unrelated asexual lineages. In accord with this finding, colonies never contained more than a single asexual lineage and average pairwise genetic relatedness within colonies was extremely high (r = 0.99). This implies that the scope for social conflict in C. biroi is limited, with unusually high potential for cooperation and altruism.
2013_kronauer_et_al.pdf Groen SC, Whiteman NK, Bahrami AK, Wilczek AM, Cui JP, Russell JA, Cibrian-Jaramillo A, Butler IA, Rana JD, Huang GH, et al. Pathogen-Triggered Ethylene Signaling Mediates Systemic-Induced Susceptibility to Herbivory in Arabidopsis. Plant Cell. 2013;25 :4755-4766.
AbstractMulticellular eukaryotic organisms are attacked by numerous parasites from diverse phyla, often simultaneously or sequentially. An outstanding question in these interactions is how hosts integrate signals induced by the attack of different parasites. We used a model system comprised of the plant host Arabidopsis thaliana, the hemibiotrophic bacterial phytopathogen Pseudomonas syringae, and herbivorous larvae of the moth Trichoplusia ni (cabbage looper) to characterize mechanisms involved in systemic-induced susceptibility (SIS) to T. ni herbivory caused by prior infection by virulent P. syringae. We uncovered a complex multilayered induction mechanism for SIS to herbivory. In this mechanism, antiherbivore defenses that depend on signaling via (1) the jasmonic acid-isoleucine conjugate (JA-Ile) and (2) other octadecanoids are suppressed by microbe-associated molecular pattern-triggered salicylic acid (SA) signaling and infection-triggered ethylene signaling, respectively. SIS to herbivory is, in turn, counteracted by a combination of the bacterial JA-Ile mimic coronatine and type III virulence-associated effectors. Our results show that SIS to herbivory involves more than antagonistic signaling between SA and JA-Ile and provide insight into the unexpectedly complex mechanisms behind a seemingly simple trade-off in plant defense against multiple enemies.
2013_groen_et_al.pdf