Publications

2014
Rabeling C, Schultz TR, Pierce NE, Bacci M. A Social Parasite Evolved Reproductive Isolation from Its Fungus-Growing Ant Host in Sympatry. Current Biology. 2014;24 :2047-2052.Abstract

Inquiline social parasitic ant species exploit colonies of other ant species mainly by producing sexual offspring that are raised by the host. Ant social parasites and their hosts are often close relatives (Emery's rule), and two main hypotheses compete to explain the parasites' evolutionary origins: (1) the interspecific hypothesis proposes an allopatric speciation scenario for the parasite, whereas (2) the intraspecific hypothesis postulates that the parasite evolves directly from its host in sympatry [1-10]. Evidence in support of the intraspecific hypothesis has been accumulating for ants [3, 5, 7, 9-12], but sympatric speciation remains controversial as a general speciation mechanism for inquiline parasites. Here we use molecular phylogenetics to assess whether the socially parasitic fungus-growing ant Mycocepurus castrator speciated from its host Mycocepurus goeldii in sympatry. Based on differing patterns of relationship in mitochondrial and individual nuclear genes, we conclude that host and parasite occupy a temporal window in which lineage sorting has taken place in the mitochondrial genes but not yet in the nuclear alleles. We infer that the host originated first and that the parasite originated subsequently from a subset of the host species' populations, providing empirical support for the hypothesis that inquiline parasites can evolve reproductive isolation while living sympatrically with their hosts.

2014_rabeling_et_al_social_parasite.pdf
Sanders JG, Powell S, Kronauer DJ, Vasconcelos HL, Frederickson ME, Pierce NE. Stability and phylogenetic correlation in gut microbiota: lessons from ants and apes. Molecular Ecology. 2014;23 :1268-83.Abstract

Correlation between gut microbiota and host phylogeny could reflect codiversification over shared evolutionary history or a selective environment that is more similar in related hosts. These alternatives imply substantial differences in the relationship between host and symbiont, but can they be distinguished based on patterns in the community data themselves? We explored patterns of phylogenetic correlation in the distribution of gut bacteria among species of turtle ants (genus Cephalotes), which host a dense gut microbial community. We used 16S rRNA pyrosequencing from 25 Cephalotes species to show that their gut community is remarkably stable, from the colony to the genus level. Despite this overall similarity, the existing differences among species' microbiota significantly correlated with host phylogeny. We introduced a novel analytical technique to test whether these phylogenetic correlations are derived from recent bacterial evolution, as would be expected in the case of codiversification, or from broader shifts more likely to reflect environmental filters imposed by factors such as diet or habitat. We also tested this technique on a published data set of ape microbiota, confirming earlier results while revealing previously undescribed patterns of phylogenetic correlation. Our results indicated a high degree of partner fidelity in the Cephalotes microbiota, suggesting that vertical transmission of the entire community could play an important role in the evolution and maintenance of the association. As additional comparative microbiota data become available, the techniques presented here can be used to explore trends in the evolution of host-associated microbial communities.

2014_sanders_et_al.pdf
Kocher SD, Pellissier L, Veller C, Purcell J, Nowak MA, Chapuisat M, Pierce NE. Transitions in social complexity along elevational gradients reveal a combined impact of season length and development time on social evolution. Proceedings of the Royal Society B-Biological Sciences. 2014;281.Abstract

Eusociality is taxonomically rare, yet associated with great ecological success. Surprisingly, studies of environmental conditions favouring eusociality are often contradictory. Harsh conditions associated with increasing altitude and latitude seem to favour increased sociality in bumblebees and ants, but the reverse pattern is found in halictid bees and polistine wasps. Here, we compare the life histories and distributions of populations of 176 species of Hymenoptera from the Swiss Alps. We show that differences in altitudinal distributions and development times among social forms can explain these contrasting patterns: highly social taxa develop more quickly than intermediate social taxa, and are thus able to complete the reproductive cycle in shorter seasons at higher elevations. This dual impact of altitude and development time on sociality illustrates that ecological constraints can elicit dynamic shifts in behaviour, and helps explain the complex distribution of sociality across ecological gradients.

2014_kocher_et_al.pdf
2013
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.Abstract

In 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.Abstract

The 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.Abstract

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.

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.Abstract

The 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.Abstract

Understanding 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.Abstract

Multicellular 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
2012
Kronauer DJC, Pierce NE, Keller L. Asexual reproduction in introduced and native populations of the ant Cerapachys biroi. Molecular Ecology. 2012;21 :5221-5235.Abstract

Asexual reproduction is particularly common among introduced species, probably because it helps to overcome the negative effects associated with low population densities during colonization. The ant Cerapachys biroi has been introduced to tropical and subtropical islands around the world since the beginning of the last century. In this species, workers can reproduce via thelytokous parthenogenesis. Here, we use genetic markers to reconstruct the history of anthropogenic introductions of C.biroi, and to address the prevalence of female parthenogenesis in introduced and native populations. We show that at least four genetically distinct lineages have been introduced from continental Asia and have led to the species' circumtropical establishment. Our analyses demonstrate that asexual reproduction dominates in the introduced range and is also common in the native range. Given that C.biroi is the only dorylomorph ant that has successfully become established outside of its native range, this unusual mode of reproduction probably facilitated the species' worldwide spread. On the other hand, the rare occurrence of haploid males and at least one clear case of sexual recombination in the introduced range show that C.biroi has not lost the potential for sex. Finally, we show that thelytoky in C.biroi probably has a genetic rather than an infectious origin, and that automixis with central fusion is the most likely underlying cytological mechanism. This is in accordance with what is known for other thelytokous eusocial Hymenoptera.

2012_kronauer_et_al_asexual_reproduction.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. 2012.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 50 ha BCI plot, with three observers walking each of 10 transects of 500 m for 30 min 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.

2012_basset_et_al_cross_continental_comparisons.pdf
Frederickson ME, Ravenscraft A, Miller GA, Hernandez LMA, Booth G, Pierce NE. The Direct and Ecological Costs of an Ant-Plant Symbiosis. American Naturalist. 2012;179 :768-778.Abstract

How strong is selection for cheating in mutualisms? The answer depends on the type and magnitude of the costs of the mutualism. Here we investigated the direct and ecological costs of plant defense by ants in the association between Cordia nodosa, a myr-mecophytic plant, and Allomerus octoarticulatus, a phytoecious ant. Cordia nodosa trees produce food and housing to reward ants that protect them against herbivores. For nearly 1 year, we manipulated the presence of A. octoarticulatus ants and most insect herbivores on C. nodosa in a full-factorial experiment. Ants increased plant growth when herbivores were present but decreased plant growth when herbivores were absent, indicating that hosting ants can be costly to plants. However, we did not detect a cost to ant colonies of defending host plants against herbivores. Although this asymmetry in costs suggests that the plants may be under stronger selection than the ants to cheat by withholding investment in their partner, the costs to C. nodosa are probably at least partly ecological, arising because ants tend scale insects on their host plants. We argue that ecological costs should favor resistance or traits other than cheating and thus that neither partner may face much temptation to cheat.

2012_frederickson_direct_and_ecological_costs.pdf
Talavera G, Lukhtanov VA, Pierce NE, Villa R. Establishing criteria for higher-level classification using molecular data: the systematics of Polyommatusblue butterflies (Lepidoptera, Lycaenidae). Cladistics. 2012 :1-27.Abstract

Most taxonomists agree on the need to adapt current classifications to recognize monophyletic units. However, delineations between higher taxonomic units can be based on the relative ages of different lineages and ⁄or the level of morphological differentiation. In this paper, we address these issues in considering the species-rich Polyommatus section, a group of butterflies whose taxonomy has been highly controversial. We propose a taxonomy-friendly, flexible temporal scheme for higher-level classification. Using molecular data from nine markers (6666 bp) for 104 representatives of the Polyommatus section, representing all but two of the 81 described genera ⁄subgenera and five outgroups, we obtained a complete and well resolved phylogeny for this clade. We use this to revise the systematics of the Polyommatus blues, and to define criteria that best accommodate the described genera within a phylogenetic framework. First, we normalize the concept of section (Polyommatus) and propose the use of subtribe (Polyommatina) instead. To preserve taxonomic stability and traditionally recognized taxa, we designate an age interval (4–5 Myr) instead of a fixed minimum age to define genera. The application of these criteria results in the retention of 31 genera of the 81 formally described generic names, and necessitates the description of one new genus (Rueckbeilia gen. nov.). We note that while classifications should be based on phylogenetic data, applying a rigid universal scheme is rarely feasible. Ideally, taxon age limits should be applied according to the particularities and pre-existing taxonomy of each group. We demonstrate that the concept of a morphological gap may be misleading at the genus level and can produce polyphyletic genera, and we propose that recognition of the existence of cryptic genera may be useful in taxonomy.

2012_talavera_et_al_polyommatus.pdf
Whiteman NK, Gloss AD, Sackton TB, Groen SC, Humphrey PT, Lapoint RT, Sonderby IE, Halkier BA, Kocks C, Ausubel FM, et al. Genes Involved in the Evolution of Herbivory by a Leaf-Mining, Drosophilid Fly. Genome Biology and Evolution. 2012;4 :900-916.Abstract

Herbivorous insects are among the most successful radiations of life. However, we know little about the processes underpinning the evolution of herbivory. We examined the evolution of herbivory in the fly, Scaptomyza flava, whose larvae are leaf miners on species of Brassicaceae, including the widely studied reference plant, Arabidopsis thaliana (Arabidopsis). Scaptomyza flava is phylogenetically nested within the paraphyletic genus Drosophila, and the whole genome sequences available for 12 species of Drosophila facilitated phylogenetic analysis and assembly of a transcriptome for S. flava. A time-calibrated phylogeny indicated that leaf mining in Scaptomyza evolved between 6 and 16 million years ago. Feeding assays showed that biosynthesis of glucosinolates, the major class of antiherbivore chemical defense compounds in mustard leaves, was upregulated by S. flava larval feeding. The presence of glucosinolates in wild-type (WT) Arabidopsis plants reduced S. flava larval weight gain and increased egg-adult development time relative to flies reared in glucosinolate knockout (GKO) plants. An analysis of gene expression differences in 5-day-old larvae reared on WT versus GKO plants showed a total of 341 transcripts that were differentially regulated by glucosinolate uptake in larval S. flava. Of these, approximately a third corresponded to homologs of Drosophila melanogaster genes associated with starvation, dietary toxin-, heat-, oxidation-, and aging-related stress. The upregulated transcripts exhibited elevated rates of protein evolution compared with unregulated transcripts. The remaining differentially regulated transcripts also contained a higher proportion of novel genes than the unregulated transcripts. Thus, the transition to herbivory in Scaptomyza appears to be coupled with the evolution of novel genes and the co-option of conserved stress-related genes.

2012_whiteman_et_al_gbe.pdf faculty_1000_recommendation_clark.jpg
Russell JA, Funaro CF, Giraldo YM, Goldman-Huertas B, Suh D, Kronauer DJC, Moreau CS, Pierce NE. A Veritable Menagerie of Heritable Bacteria from Ants, Butterflies, and Beyond: Broad Molecular Surveys and a Systematic Review. Plos One. 2012;7.Abstract

Maternally transmitted bacteria have been important players in the evolution of insects and other arthropods, affecting their nutrition, defense, development, and reproduction. Wolbachia are the best studied among these and typically the most prevalent. While several other bacteria have independently evolved a heritable lifestyle, less is known about their host ranges. Moreover, most groups of insects have not had their heritable microflora systematically surveyed across a broad range of their taxonomic diversity. To help remedy these shortcomings we used diagnostic PCR to screen for five groups of heritable symbionts-Arsenophonus spp., Cardinium hertigii, Hamiltonella defensa, Spiroplasma spp., and Wolbachia spp.-across the ants and lepidopterans (focusing, in the latter case, on two butterfly families-the Lycaenidae and Nymphalidae). We did not detect Cardinium or Hamiltonella in any host. Wolbachia were the most widespread, while Spiroplasma (ants and lepidopterans) and Arsenophonus (ants only) were present at low levels. Co-infections with different Wolbachia strains appeared especially common in ants and less so in lepidopterans. While no additional facultative heritable symbionts were found among ants using universal bacterial primers, microbes related to heritable enteric bacteria were detected in several hosts. In summary, our findings show that Wolbachia are the dominant heritable symbionts of ants and at least some lepidopterans. However, a systematic review of symbiont frequencies across host taxa revealed that this is not always the case across other arthropods. Furthermore, comparisons of symbiont frequencies revealed that the prevalence of Wolbachia and other heritable symbionts varies substantially across lower-level arthropod taxa. We discuss the correlates, potential causes, and implications of these patterns, providing hypotheses on host attributes that may shape the distributions of these influential bacteria.

2012_russell_et_al_veritable_menagerie.pdf
2011
Funaro CF, Kronauer DJC, Moreau CS, Goldman-Huertas B, Pierce NE, Russell JA. Army Ants Harbor a Host-Specific Clade of Entomoplasmatales Bacteria. Applied and Environmental Microbiology. 2011;77 :346-350.Abstract

In this article, we describe the distributions of Entomoplasmatales bacteria across the ants, identifying a novel lineage of gut bacteria that is unique to the army ants. While our findings indicate that the Entomoplasmatales are not essential for growth or development, molecular analyses suggest that this relationship is host specific and potentially ancient. The documented trends add to a growing body of literature that hints at a diversity of undiscovered associations between ants and bacterial symbionts.

2011_funaro_et_al.pdf
Ramirez SR, Eltz T, Fujiwara MK, Gerlach G, Goldman-Huertas B, Tsutsui ND, Pierce NE. Asynchronous Diversification in a Specialized Plant-Pollinator Mutualism. Science. 2011;333 :1742-1746.Abstract

Most flowering plants establish mutualistic associations with insect pollinators to facilitate sexual reproduction. However, the evolutionary processes that gave rise to these associations remain poorly understood. We reconstructed the times of divergence, diversification patterns, and interaction networks of a diverse group of specialized orchids and their bee pollinators. In contrast to a scenario of coevolution by race formation, we show that fragrance-producing orchids originated at least three times independently after their fragrance-collecting bee mutualists. Whereas orchid diversification has apparently tracked the diversification of orchids' bee pollinators, bees appear to have depended on the diverse chemical environment of neotropical forests. We corroborated this apparent asymmetrical dependency by simulating co-extinction cascades in real interaction networks that lacked reciprocal specialization. These results suggest that the diversification of insect-pollinated angiosperms may have been facilitated by the exploitation of preexisting sensory biases of insect pollinators.

2011_ramirez_et_al.pdf
Archetti M, Scheuring I, Hoffman M, Frederickson ME, Pierce NE, Yu DW. Economic game theory for mutualism and cooperation. Ecology Letters. 2011;14 :1300-1312.Abstract

We review recent work at the interface of economic game theory and evolutionary biology that provides new insights into the evolution of partner choice, host sanctions, partner fidelity feedback and public goods. (1) The theory of games with asymmetrical information shows that the right incentives allow hosts to screen-out parasites and screen-in mutualists, explaining successful partner choice in the absence of signalling. Applications range from ant-plants to microbiomes. (2) Contract theory distinguishes two longstanding but weakly differentiated explanations of host response to defectors: host sanctions and partner fidelity feedback. Host traits that selectively punish misbehaving symbionts are parsimoniously interpreted as pre-adaptations. Yucca-moth and legume-rhizobia mutualisms are argued to be examples of partner fidelity feedback. (3) The theory of public goods shows that cooperation in multi-player interactions can evolve in the absence of assortment, in one-shot social dilemmas among non-kin. Applications include alarm calls in vertebrates and exoenzymes in microbes.

archetti_et_al-2011-ecology_letters.pdf
Pierce NE, Berry AJ. The herbivore's dilemma: Never enough nitrogen. In: Losos J (ed) In the Light of Evolution: Essays From the Laboratory and Field. 1st ed. Roberts & Company ; 2011. pp. 121-134. 2011_pierce_berry_herbivores_dilemma.pdf

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