• Ancient RNA virus epidemics through the lens of recent adaptation in human genomes

      Enard, David; Petrov, Dmitri A; Univ Arizona, Dept Ecol & Evolutionary Biol (ROYAL SOC, 2020-10-05)
      Over the course of the last several million years of evolution, humans probably have been plagued by hundreds or perhaps thousands of epidemics. Little is known about such ancient epidemics and a deep evolutionary perspective on current pathogenic threats is lacking. The study of past epidemics has typically been limited in temporal scope to recorded history, and in physical scope to pathogens that left sufficient DNA behind, such as Yersinia pestis during the Great Plague. Host genomes, however, offer an indirect way to detect ancient epidemics beyond the current temporal and physical limits. Arms races with pathogens have shaped the genomes of the hosts by driving a large number of adaptations at many genes, and these signals can be used to detect and further characterize ancient epidemics. Here, we detect the genomic footprints left by ancient viral epidemics that took place in the past approximately 50 000 years in the 26 human populations represented in the 1000 Genomes Project. By using the enrichment in signals of adaptation at approximately 4500 host loci that interact with specific types of viruses, we provide evidence that RNA viruses have driven a particularly large number of adaptive events across diverse human populations. These results suggest that different types of viruses may have exerted different selective pressures during human evolution. Knowledge of these past selective pressures will provide a deeper evolutionary perspective on current pathogenic threats. This article is part of the theme issue 'Insights into health and disease from ancient biomolecules'.
    • Anthropogenic impacts drive niche and conservation metrics of a cryptic rattlesnake on the Colorado Plateau of western North America

      Douglas, M. R.; Davis, M. A.; Amarello, M.; Smith, J. J.; Schuett, G. W.; Herrmann, H.-W.; Holycross, A. T.; Douglas, M. E.; Univ Arizona, Nat Resources & Environm (ROYAL SOC, 2016-04-27)
      Ecosystems transition quickly in the Anthropocene, whereas biodiversity adapts more slowly. Here we simulated a shifting woodland ecosystem on the Colorado Plateau of western North America by using as its proxy over space and time the fundamental niche of the Arizona black rattlesnake (Crotalus cerberus). We found an expansive (= end-of-Pleistocene) range that contracted sharply (= present), but is blocked topographically by Grand Canyon/Colorado River as it shifts predictably northwestward under moderate climate change (= 2080). Vulnerability to contemporary wildfire was quantified from available records, with forested area reduced more than 27% over 13 years. Both 'ecosystem metrics' underscore how climate and wildfire are rapidly converting the Plateau ecosystem into novel habitat. To gauge potential effects on C. cerberus, we derived a series of relevant 'conservation metrics' (i.e. genetic variability, dispersal capacity, effective population size) by sequencing 118 individuals across 846 bp of mitochondrial (mt)DNA-ATPase8/6. We identified five significantly different clades (net sequence divergence = 2.2%) isolated by drainage/topography, with low dispersal (F-ST = 0.82) and small sizes (2N(ef) = 5.2). Our compiled metrics (i.e. small-populations, topographic-isolation, low-dispersal versus conserved-niche, vulnerable-ecosystem, dispersal barriers) underscore the susceptibility of this woodland specialist to a climate and wildfire tandem. We offer adaptive management scenarios that may counterbalance these metrics and avoid the extirpation of this and other highly specialized, relictual woodland clades.
    • Do-it-yourself networks: a novel method of generating weighted networks

      Shanafelt, D. W.; Salau, K. R.; Baggio, J. A.; Univ Arizona, Dept Math (ROYAL SOC, 2017-11-22)
      Network theory is finding applications in the life and social sciences for ecology, epidemiology, finance and social-ecological systems. While there are methods to generate specific types of networks, the broad literature is focused on generating unweighted networks. In this paper, we present a framework for generating weighted networks that satisfy user- defined criteria. Each criterion hierarchically defines a feature of the network and, in doing so, complements existing algorithms in the literature. We use a general example of ecological species dispersal to illustrate the method and provide open- source code for academic purposes.
    • Evaluating a transfer gradient assumption in a fomite-mediated microbial transmission model using an experimental and Bayesian approach

      Wilson, Amanda M; King, Marco-Felipe; López-García, Martín; Weir, Mark H; Sexton, Jonathan D; Canales, Robert A; Kostov, Georgiana E; Julian, Timothy R; Noakes, Catherine J; Reynolds, Kelly A; et al. (ROYAL SOC, 2020-06-24)
      Current microbial exposure models assume that microbial exchange follows a concentration gradient during hand-to-surface contacts. Our objectives were to evaluate this assumption using transfer efficiency experiments and to evaluate a model's ability to explain concentration changes using approximate Bayesian computation (ABC) on these experimental data. Experiments were conducted with two phages (MS2, ΦX174) simultaneously to study bidirectional transfer. Concentrations on the fingertip and surface were quantified before and after fingertip-to-surface contacts. Prior distributions for surface and fingertip swabbing efficiencies and transfer efficiency were used to estimate concentrations on the fingertip and surface post contact. To inform posterior distributions, Euclidean distances were calculated for predicted detectable concentrations (log10 PFU cm-2) on the fingertip and surface post contact in comparison with experimental values. To demonstrate the usefulness of posterior distributions in calibrated model applications, posterior transfer efficiencies were used to estimate rotavirus infection risks for a fingertip-to-surface and subsequent fingertip-to-mouth contact. Experimental findings supported the transfer gradient assumption. Through ABC, the model explained concentration changes more consistently when concentrations on the fingertip and surface were similar. Future studies evaluating microbial transfer should consider accounting for differing fingertip-to-surface and surface-to-fingertip transfer efficiencies and extend this work for other microbial types.
    • Evolution of long-term coloration trends with biochemically unstable ingredients

      Higginson, Dawn M.; Belloni, Virginia; Davis, Sarah N.; Morrison, Erin S.; Andrews, John E.; Badyaev, Alexander V.; Univ Arizona, Dept Ecol & Evolutionary Biol (ROYAL SOC, 2016-05-18)
      The evolutionarily persistent and widespread use of carotenoid pigments in animal coloration contrasts with their biochemical instability. Consequently, evolution of carotenoid-based displays should include mechanisms to accommodate or limit pigment degradation. In birds, this could involve two strategies: (i) evolution of a moult immediately prior to the mating season, enabling the use of particularly fast-degrading carotenoids and (ii) evolution of the ability to stabilize dietary carotenoids through metabolic modification or association with feather keratins. Here, we examine evolutionary lability and transitions between the two strategies across 126 species of birds. We report that species that express mostly unmodified, fast-degrading, carotenoids have pre-breeding moults, and a particularly short time between carotenoid deposition and the subsequent breeding season. Species that expressed mostly slow-degrading carotenoids in their plumage accomplished this through increased metabolic modification of dietary carotenoids, and the selective expression of these slow-degrading compounds. In these species, the timing of moult was not associated with carotenoid composition of plumage displays. Using repeated samples from individuals of one species, we found that metabolic modification of dietary carotenoids significantly slowed their degradation between moult and breeding season. Thus, the most complex and colourful ornamentation is likely the most biochemically stable in birds, and depends less on ecological factors, such as moult timing and migration tendency. We suggest that coevolution of metabolic modification, selective expression and biochemical stability of plumage carotenoids enables the use of unstable pigments in long-term evolutionary trends in plumage coloration.
    • Exploration of pathomechanisms triggered by a single-nucleotide polymorphism in titin's I-band: the cardiomyopathy-linked mutation T2580I

      Bogomolovas, Julius; Fleming, Jennifer R.; Anderson, Brian R.; Williams, Rhys; Lange, Stephan; Simon, Bernd; Khan, Muzamil M.; Rudolf, Rüdiger; Franke, Barbara; Bullard, Belinda; et al. (ROYAL SOC, 2016-09-28)
      Missense single-nucleotide polymorphisms (mSNPs) in titin are emerging as a main causative factor of heart failure. However, distinguishing between benign and disease-causing mSNPs is a substantial challenge. Here, we research the question of whether a single mSNP in a generic domain of titin can affect heart function as a whole and, if so, how. For this, we studied the mSNP T2850I, seemingly linked to arrhythmogenic right ventricular cardiomyopathy (ARVC). We used structural biology, computational simulations and transgenic muscle in vivo methods to track the effect of the mutation from the molecular to the organismal level. The data show that the T2850I exchange is compatible with the domain three-dimensional fold, but that it strongly destabilizes it. Further, it induces a change in the conformational dynamics of the titin chain that alters its reactivity, causing the formation of aberrant interactions in the sarcomere. Echocardiography of knock-in mice indicated a mild diastolic dysfunction arising from increased myocardial stiffness. In conclusion, our data provide evidence that single mSNPs in titin's I-band can alter overall muscle behaviour. Our suggested mechanisms of disease are the development of non-native sarcomeric interactions and titin instability leading to a reduced I-band compliance. However, understanding the T2850I-induced ARVC pathology mechanistically remains a complex problem and will require a deeper understanding of the sarcomeric context of the titin region affected.
    • Fossil clam shells reveal unintended carbon cycling consequences of Colorado River management

      Smith, Jansen A.; Auerbach, Daniel A.; Flessa, Karl W.; Flecker, Alexander S.; Dietl, Gregory P.; Univ Arizona, Dept Geosci (ROYAL SOC, 2016-09-28)
      Water management that alters riverine ecosystem processes has strongly influenced deltas and the people who depend on them, but a full accounting of the trade-offs is still emerging. Using palaeoecological data, we document a surprising biogeochemical consequence of water management in the Colorado River basin. Complete allocation and consumptive use of the river's flow has altered the downstream estuarine ecosystem, including the abundance and composition of the mollusc community, an important component in estuarine carbon cycling. In particular, population declines in the endemic Colorado delta clam, Mulinia coloradoensis, from 50-125 individuals m(-2) in the pre-dam era to three individualsm-2 today, have likely resulted in a reduction, on the order of 5900-15 000 tCyr(-1) (4.1-10.6 mol Cm-2 yr(-1)), in the net carbon emissions associated with molluscs. Although this reduction is large within the estuarine system, it is small in comparison with annual global carbon emissions. Nonetheless, this finding highlights the need for further research into the effects of dams, diversions and reservoirs on the biogeochemistry of deltas and estuaries worldwide, underscoring a present need for integrated water and carbon planning.
    • Highly heritable and functionally relevant breed differences in dog behaviour

      MacLean, Evan L; Snyder-Mackler, Noah; vonHoldt, Bridgett M; Serpell, James A; Univ Arizona, Sch Anthropol; Univ Arizona, Dept Psychol (ROYAL SOC, 2019-10-02)
      Variation across dog breeds presents a unique opportunity to investigate the evolution and biological basis of complex behavioural traits. We integrated behavioural data from more than 14 000 dogs from 101 breeds with breed-averaged genotypic data (n = 5697 dogs) from over 100 000 loci in the dog genome. We found high levels of among-breed heritability for 14 behavioural traits (the proportion of trait variance attributable to genetic similarity among breeds). We next identified 131 single nucleotide polymorphisms associated with breed differences in behaviour, which were found in genes that are highly expressed in the brain and enriched for neurobiological functions and developmental processes, suggesting that they may be functionally associated with behavioural differences. Our results shed light on the heritability and genetic architecture of complex behavioural traits and identify dogs as a powerful model in which to address these questions.
    • A highly infective plant-associated bacterium influences reproductive rates in pea aphids

      Hendry, Tory A.; Clark, Kelley J.; Baltrus, David A.; Univ Arizona, Sch Plant Sci (ROYAL SOC, 2016-02-10)
      Pea aphids, Acyrthosiphon pisum, have the potential to increase reproduction as a defence against pathogens, though how frequently this occurs or how infection with live pathogens influences this response is not well understood. Here we determine the minimum infective dose of an environmentally common bacterium and possible aphid pathogen, Pseudomonas syringae, to determine the likelihood of pathogenic effects to pea aphids. Additionally, we used P. syringae infection to investigate how live pathogens may alter reproductive rates. We found that oral bacterial exposure decreased subsequent survival of aphids in a dose-dependent manner and we estimate that ingestion of less than 10 bacterial cells is sufficient to increase aphid mortality. Pathogen dose was positively related to aphid reproduction. Aphids exposed to low bacterial doses showed decreased, although statistically indistinguishable, fecundity compared to controls. Aphids exposed to high doses reproduced significantly more than low dose treatments and also more, but not significantly so, than controls. These results are consistent with previous studies suggesting that pea aphids may use fecundity compensation as a response to pathogens. Consequently, even low levels of exposure to a common plant-associated bacterium may therefore have significant effects on pea aphid survival and reproduction.
    • Humans permanently occupied the Andean highlands by at least 7 ka

      Haas, Randall; Stefanescu, Ioana C.; Garcia-Putnam, Alexander; Aldenderfer, Mark S.; Clementz, Mark T.; Murphy, Melissa S.; Llave, Carlos Viviano; Watson, James T.; Univ Arizona, Arizona State Museum; Univ Arizona, Sch Anthropol (ROYAL SOC, 2017-06-28)
      High-elevation environments above 2500 metres above sea level (m.a.s.l.) were among the planet's last frontiers of human colonization. Research on the speed and tempo of this colonization process is active and holds implications for understanding rates of genetic, physiological and cultural adaptation in our species. Permanent occupation of high-elevation environments in the Andes Mountains of South America tentatively began with hunter-gatherers around 9 ka according to current archaeological estimates, though the timing is currently debated. Recent observations on the archaeological site of Soro Mik'aya Patjxa (8.0-6.5 ka), located at 3800 m.a.s.l. in the Andean Altiplano, offer an opportunity to independently test hypotheses for early permanent use of the region. This study observes low oxygen (delta O-18) and high carbon (delta C-13) isotope values in human bone, long travel distances to low-elevation zones, variable age and sex structure in the human population and an absence of non-local lithic materials. These independent lines of evidence converge to support a model of permanent occupation of high elevations and refute logistical and seasonal use models. The results constitute the strongest empirical support to date for permanent human occupation of the Andean highlands by hunter-gatherers before 7 ka.
    • Influence of local and landscape factors on distributional dynamics: a species-centred, fitness-based approach

      Flesch, Aaron D.; Univ Arizona, Sch Nat Resources & Environm, Desert Lab (ROYAL SOC, 2017-07-05)
      In spatially structured populations, distributional dynamics are driven by the quantity, connectivity and quality of habitat. Because these drivers are rarely measured directly and simultaneously at relevant scales, information on their relative importance remains unclear. I assessed the influence of both direct and indirect measures of local habitat quality, and of landscape habitat amount and connectivity on long-term territory occupancy dynamics of non-migratory pygmy owls. Direct measures of local habitat quality based on territory-specific reproductive output had greater effects on distribution than landscape factors, but only when spatio-temporal fluxes in performance linked to environmental stochasticity and intraspecific competition were considered. When habitat quality was measured indirectly based on habitat structure, however, landscape factors had greater effects. Although all landscape factors were important, measures of landscape connectivity that were uncorrelated with habitat amount and based on attributes of matrix structure and habitat configuration that influence dispersal movements had greater effects than habitat effective area (amount weighted by quality). Moreover, the influence of connectivity (but not habitat effective area) depended on local habitat quality. Such results suggest the relative importance of local habitat quality in driving distribution has been underestimated and that conservation strategies should vary spatially depending on both local and landscape contexts.
    • Lack of aggression and apparent altruism towards intruders in a primitive termite

      Cooney, Feargus; Vitikainen, Emma I. K.; Marshall, Harry H.; van Rooyen, Wilmie; Smith, Robert L.; Cant, Michael A.; Goodey, Nicole; Univ Arizona, Dept Entomol (ROYAL SOC, 2016-11-09)
      In eusocial insects, the ability to discriminate nest-mates from non-nest-mates is widespread and ensures that altruistic actions are directed towards kin and agonistic actions are directed towards non-relatives. Most tests of nest-mate recognition have focused on hymenopterans, and suggest that cooperation typically evolves in tandem with strong antagonism towards non-nest-mates. Here, we present evidence from a phylogenetically and behaviourally basal termite species that workers discriminate members of foreign colonies. However, contrary to our expectations, foreign intruders were the recipients of more rather than less cooperative behaviour and were not subjected to elevated aggression. We suggest that relationships between groups may be much more peaceable in basal termites compared with eusocial hymenoptera, owing to energetic and temporal constraints on colony growth, and the reduced incentive that totipotent workers (who may inherit breeding status) have to contribute to self-sacrificial intergroup conflict.
    • Marine mammal skin microbiotas are influenced by host phylogeny

      Apprill, Amy; Miller, Carolyn A; Van Cise, Amy M; U'Ren, Jana M; Leslie, Matthew S; Weber, Laura; Baird, Robin W; Robbins, Jooke; Landry, Scott; Bogomolni, Andrea; et al. (ROYAL SOC, 2020-05-20)
      Skin-associated microorganisms have been shown to play a role in immune function and disease of humans, but are understudied in marine mammals, a diverse animal group that serve as sentinels of ocean health. We examined the microbiota associated with 75 epidermal samples opportunistically collected from nine species within four marine mammal families, including: Balaenopteridae (sei and fin whales), Phocidae (harbour seal), Physeteridae (sperm whales) and Delphinidae (bottlenose dolphins, pantropical spotted dolphins, rough-toothed dolphins, short-finned pilot whales and melon-headed whales). The skin was sampled from free-ranging animals in Hawai'i (Pacific Ocean) and off the east coast of the United States (Atlantic Ocean), and the composition of the bacterial community was examined using the sequencing of partial small subunit (SSU) ribosomal RNA genes. Skin microbiotas were significantly different among host species and taxonomic families, and microbial community distance was positively correlated with mitochondrial-based host genetic divergence. The oceanic location could play a role in skin microbiota variation, but skin from species sampled in both locations is necessary to determine this influence. These data suggest that a phylosymbiotic relationship may exist between microbiota and their marine mammal hosts, potentially providing specific health and immune-related functions that contribute to the success of these animals in diverse ocean ecosystems.
    • Mie scattering and microparticle-based characterization of heavy metal ions and classification by statistical inference methods

      Klug, Katherine E; Jennings, Christian M; Lytal, Nicholas; An, Lingling; Yoon, Jeong-Yeol; Univ Arizona, Dept Biosyst Engn; Univ Arizona, Dept Biomed Engn; Univ Arizona, Stat Grad Interdisciplinary Program; Univ Arizona, Dept Biostat & Epidemiol (ROYAL SOC, 2019-05)
      A straightforward method for classifying heavy metal ions in water is proposed using statistical classification and clustering techniques from non-specific microparticle scattering data. A set of carboxylated polystyrene microparticles of sizes 0.91, 0.75 and 0.40 mu m was mixed with the solutions of nine heavy metal ions and two control cations, and scattering measurements were collected at two angles optimized for scattering from non-aggregated and aggregated particles. Classification of these observations was conducted and compared among several machine learning techniques, including linear discriminant analysis, support vector machine analysis, K-means clustering and K-medians clustering. This study found the highest classification accuracy using the linear discriminant and support vector machine analysis, each reporting high classification rates for heavy metal ions with respect to the model. This may be attributed to moderate correlation between detection angle and particle size. These classification models provide reasonable discrimination between most ion species, with the highest distinction seen for Pb(II), Cd(II), Ni(II) and Co(II), followed by Fe(II) and Fe(III), potentially due to its known sorption with carboxyl groups. The support vector machine analysis was also applied to three different mixture solutions representing leaching from pipes and mine tailings, and showed good correlation with single-species data, specifically with Pb(II) and Ni(II). With more expansive training data and further processing, this method shows promise for low-cost and portable heavy metal identification and sensing.
    • A new terrestrial palaeoenvironmental record from the Bering Land Bridge and context for human dispersal

      Wooller, Matthew J.; Saulnier-Talbot, Émilie; Potter, Ben A.; Belmecheri, Soumaya; Bigelow, Nancy; Choy, Kyungcheol; Cwynar, Les C.; Davies, Kimberley; Graham, Russell W.; Kurek, Joshua; et al. (ROYAL SOC, 2018-06)
      Palaeoenvironmental records from the now-submerged Bering Land Bridge (BLB) covering the Last Glacial Maximum (LGM) to the present are needed to document changing environments and connections with the dispersal of humans into North America, Moreover, terrestrially based records of environmental changes are needed in close proximity to the re-establishment of circulation between Pacific and Atlantic Oceans following the end of the last glaciation to test palaeo-dimate models for the high latitudes. We present the first terrestrial temperature and hydrologic reconstructions from the LGM to the present from the BLB's south-central margin. We find that the timing of the earliest unequivocal human dispersals into Alaska, based on archaeological evidence, corresponds with a shift to warmer/wetter conditions on the BLB between 14700 and 13500 years ago associated with the early Balling/Aliened interstadial (BA), These environmental changes could have provided the impetus for eastward human dispersal at that time, from Western or central Beringia after a protracted human population standstill. Our data indicate substantial climate-induced environmental changes on the BLB since the LGM, which would potentially have had significant influences on megafaunal and human biogeography in the region.
    • No evidence of male-biased sexual selection in a snake with conventional Darwinian sex roles

      Levine, Brenna A.; Schuett, Gordon W.; Clark, Rulon W.; Repp, Roger A.; Herrmann, Hans-Werner; Booth, Warren; Univ Arizona, Sch Nat Resources & Environm (ROYAL SOC, 2020-10-07)
      Decades of research on sexual selection have demonstrated that 'conventional' Darwinian sex roles are common in species with anisogamous gametes, with those species often exhibiting male-biased sexual selection. Yet, mating system characteristics such as long-term sperm storage and polyandry have the capacity to disrupt this pattern. Here, these ideas were explored by quantifying sexual selection metrics for the western diamond-backed rattlesnake (Crotalus atrox). A significant standardized sexual selection gradient was not found for males (beta (SS) = 0.588, p = 0.199) or females (beta (SS) = 0.151, p = 0.664), and opportunities for sexual selection (I-s) and selection (I) did not differ between males (I-s = 0.069, I = 0.360) and females (I-s = 0.284, I = 0.424; both p > 0.05). Furthermore, the sexes did not differ in the maximum intensity of precopulatory sexual selection (males: s ' (max) = 0.155, females: s ' (max) = 0.080; p > 0.05). Finally, there was no evidence that male snout-vent length, a trait associated with mating advantage, is a target of sexual selection (p > 0.05). These results suggest a lack of male-biased sexual selection in this population. Mating system characteristics that could erode male-biased sexual selection, despite the presence of conventional Darwinian sex roles, are discussed.
    • Noisy communities and signal detection: why do foragers visit rewardless flowers?

      Lichtenberg, Elinor M; Heiling, Jacob M; Bronstein, Judith L; Barker, Jessica L; Univ Arizona, Dept Ecol & Evolutionary Biol (ROYAL SOC, 2020-05-18)
      Floral communities present complex and shifting resource landscapes for flower-foraging animals. Strong similarities among the floral displays of different plant species, paired with high variability in reward distributions across time and space, can weaken correlations between floral signals and reward status. As a result, it should be difficult for foragers to discriminate between rewarding and rewardless flowers. Building on signal detection theory in behavioural ecology, we use hypothetical probability density functions to examine graphically how plant signals pose challenges to forager decision-making. We argue that foraging costs associated with incorrect acceptance of rewardless flowers and incorrect rejection of rewarding ones interact with community-level reward availability to determine the extent to which rewardless and rewarding species should overlap in flowering time. We discuss the evolutionary consequences of these phenomena from both the forager and the plant perspectives. This article is part of the theme issue 'Signal detection theory in recognition systems: from evolving models to experimental tests'.
    • A novel proof of concept for capturing the diversity of endophytic fungi preserved in herbarium specimens

      Daru, Barnabas H.; Bowman, Elizabeth A.; Pfister, Donald H.; Arnold, A. Elizabeth; Univ Arizona, Sch Plant Sci; Univ Arizona, Dept Ecol & Evolutionary Biol (ROYAL SOC, 2019-01-07)
      Herbarium specimens represent important records of morphological and genetic diversity of plants that inform questions relevant to global change, including species distributions, phenology and functional traits. It is increasingly appreciated that plant microbiomes can influence these aspects of plant biology, but little is known regarding the historic distribution of microbes associated with plants collected in the pre-molecular age. If microbiomes can be observed reliably in herbarium specimens, researchers will gain a new lens with which to examine microbial ecology, evolution, species interactions. Here, we describe a method for accessing historical plant microbiomes from preserved herbarium specimens, providing a proof of concept using two plant taxa from the imperiled boreal biome (Andromeda polifolia and Ledum palustre subsp. groenlandicum, Ericaceae). We focus on fungal endophytes, which occur within symptomless plant tissues such as leaves. Through a three-part approach (i.e. culturing, cloning and next-generation amplicon sequencing via the Illumina MiSeq platform, with extensive controls), we examined endophyte communities in dried, pressed leaves that had been processed as regular herbarium specimens and stored at room temperature in a herbarium for four years. We retrieved only one endophyte in culture, but cloning and especially the MiSeq analysis revealed a rich community of foliar endophytes. The phylogenetic distribution and diversity of endophyte assemblages, especially among the Ascomycota, resemble endophyte communities from fresh plants collected in the boreal biome. We could distinguish communities of endophytes in each plant species and differentiate likely endophytes from fungi that could be surface contaminants. Taxa found by cloning were observed in the larger MiSeq dataset, but species richness was greater when subsets of the same tissues were evaluated with the MiSeq approach. Our findings provide a proof of concept for capturing endophyte DNA from herbarium specimens, supporting the importance of herbarium records as roadmaps for understanding the dynamics of plant-associated microbial biodiversity in the Anthropocene. This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.
    • Social complexity influences brain investment and neural operation costs in ants

      Kamhi, J. Frances; Gronenberg, Wulfila; Robson, Simon K. A.; Traniello, James F. A.; Univ Arizona, Dept Neurosci (ROYAL SOC, 2016-10-19)
      The metabolic expense of producing and operating neural tissue required for adaptive behaviour is considered a significant selective force in brain evolution. In primates, brain size correlates positively with group size, presumably owing to the greater cognitive demands of complex social relationships in large societies. Social complexity in eusocial insects is also associated with large groups, as well as collective intelligence and division of labour among sterile workers. However, superorganism phenotypes may lower cognitive demands on behaviourally specialized workers resulting in selection for decreased brain size and/or energetic costs of brain metabolism. To test this hypothesis, we compared brain investment patterns and cytochrome oxidase (COX) activity, a proxy for ATP usage, in two ant species contrasting in social organization. Socially complex Oecophylla smaragdina workers had larger brain size and relative investment in the mushroom bodies (MBs)-higher order sensory processing compartments-than the more socially basic Formica subsericea workers. Oecophylla smaragdina workers, however, had reduced COX activity in the MBs. Our results suggest that as in primates, ant group size is associated with large brain size. The elevated costs of investment in metabolically expensive brain tissue in the socially complex O. smaragdina, however, appear to be offset by decreased energetic costs.