Five decades of misunderstanding in the social Hymenoptera: a review and meta-analysis of Michener's paradox.

In a much-cited 1964 paper entitled "Reproductive efficiency in relation to colony size in hymenopterous societies," Charles Michener investigated the correlation between a colony's size and its reproductive efficiency - the ability of its adult females to produce reproductives, measured as per-capita output. Based on his analysis of published data from destructively sampled colonies in 18 species, he reported that in most of these species efficiency decreased with increasing colony size. His conclusion that efficiency is higher in smaller groups has since gained widespread acceptance. But it created a seeming paradox: how can natural selection maintain social behaviour when a female apparently enjoys her highest per-capita output by working alone? Here we treat Michener's pattern as a hypothesis and perform the first large-scale test of its prediction across the eusocial Hymenoptera. Because data on actual output of reproductives were not available for most species, Michener used various proxies, such as nest size, numbers of brood, or amounts of stored food. We show that for each of Michener's data sets the reported decline in per-capita productivity can be explained by factors other than decreasing efficiency, calling into question his conclusion that declining efficiency is the cause of the pattern. The most prominent cause of bias is the failure of the proxy to capture all forms of output in which the colony invests during the course of its ontogeny. Other biasing factors include seasonal effects and a variety of methodological flaws in the data sets he used. We then summarize the results of 215 data sets drawn from post-1964 studies of 80 species in 33 genera that better control for these factors. Of these, 163 data sets are included in two meta-analyses that statistically synthesize the available data on the relationship between colony size and efficiency, accounting for variable sample sizes and non-independence among the data sets. The overall effect, and those for most taxonomic subgroups, indicates no loss of efficiency with increasing colony size. Two exceptional taxa, the halictid bees and independent-founding paper wasps, show negative trends consistent with the Michener hypothesis in some species. We conclude that in most species, particularly those with large colony sizes, the hypothesis of decreasing efficiency with increasing colony size is not supported. Finally, we explore potential mechanisms through which the level of efficiency can decrease, be maintained, or even increase, as colonies increase in size.

Physical models have gender-specific effects on student understanding of protein structure-function relationships.

Understanding how basic structural units influence function is identified as a foundational/core concept for undergraduate biological and biochemical literacy. It is essential for students to understand this concept at all size scales, but it is often more difficult for students to understand structure-function relationships at the molecular level, which they cannot as effectively visualize. Students need to develop accurate, 3-dimensional mental models of biomolecules to understand how biomolecular structure affects cellular functions at the molecular level, yet most traditional curricular tools such as textbooks include only 2-dimensional representations. We used a controlled, backward design approach to investigate how hand-held physical molecular model use affected students' ability to logically predict structure-function relationships. Brief (one class period) physical model use increased quiz score for females, whereas there was no significant increase in score for males using physical models. Females also self-reported higher learning gains in their understanding of context-specific protein function. Gender differences in spatial visualization may explain the gender-specific benefits of physical model use observed. © 2016 The Authors Biochemistry and Molecular Biology Education published by Wiley Periodicals, Inc. on behalf of International Union of Biochemistry and Molecular Biology, 44(4):326-335, 2016.

The Impact of Parenthetical Phrases on Interviewers' and Respondents' Processing of Survey Questions.

Many surveys contain sets of questions (e.g., batteries), in which the same phrase, such as a reference period or a set of response categories, applies across the set. When formatting questions for interviewer administration, question writers often enclose these repeated phrases in parentheses to signal that interviewers have the option of reading the phrase. Little research, however, examines what impact this practice has on data quality. We explore whether the presence and use of parenthetical statements is associated with indicators of processing problems for both interviewers and respondents, including the interviewer's ability to read the question exactly as worded, and the respondent's ability to answer the question without displaying problems answering (e.g., expressing uncertainty). Data are from questions about physical and mental health from 355 digitally recorded, transcribed, and interaction-coded telephone interviews. We implement a mixed-effects model with crossed random effects and nested and crossed fixed effects. The models also control for some respondent and interviewer characteristics. Findings indicate respondents are less likely to exhibit a problem when parentheticals are read, but reading the parentheticals increase the odds (marginally significant) that interviewers will make a reading error.

The cues have it; nest-based, cue-mediated recruitment to carbohydrate resources in a swarm-founding social wasp.

This study explores whether or not foragers of the Neotropical swarm-founding wasp Polybia occidentalis use nest-based recruitment to direct colony mates to carbohydrate resources. Recruitment allows social insect colonies to rapidly exploit ephemeral resources, an ability especially advantageous to species such as P. occidentalis, which store nectar and prey in their nests. Although recruitment is often defined as being strictly signal mediated, it can also occur via cue-mediated information transfer. Previous studies indicated that P. occidentalis employs local enhancement, a type of cue-mediated recruitment in which the presence of conspecifics at a site attracts foragers. This recruitment is resource-based, and as such, is a blunt recruitment tool, which does not exclude non-colony mates. We therefore investigated whether P. occidentalis also employs a form of nest-based recruitment. A scented sucrose solution was applied directly to the nest. This mimicked a scented carbohydrate resource brought back by employed foragers, but, as foragers were not allowed to return to the nest with the resource, there was no possibility for on-nest recruitment behavior. Foragers were offered two dishes--one containing the test scent and the other an alternate scent. Foragers chose the test scent more often, signifying that its presence in the nest induces naïve foragers to search for it off-nest. P. occidentalis, therefore, employs a form of nest-based recruitment to carbohydrate resources that is mediated by a cue, the presence of a scented resource in the nest.

Estimation and confidence regions for multi-dimensional effective dose.

The problem of finding confidence regions for multiple predictor variables corresponding to given expected values of a response variable has not been adequately resolved. Motivated by an example from a study on hyperbaric exposure using a logistic regression model, we develop a conceptual framework for the estimation of the multi-dimensional effective dose for binary outcomes. The k -dimensional effective dose can be determined by conditioning on k - 1 components and solving for the last component as a conditional univariate effective dose. We consider various approaches for calculating confidence regions for the multi-dimensional effective dose and compare them via a simulation study for a range of possible designs. We analyze data related to decompression sickness to illustrate our procedure. Our results provide a practical approach to finding confidence regions for predictor variables for a given response value.

Dispersal, density dependence, and population dynamics of a fungal microbe on leaf surfaces.

Despite the ubiquity and importance of microbes in nature, little is known about their natural population dynamics, especially for those that occupy terrestrial habitats. Here we investigate the dynamics of the yeast-like fungus Aureobasidium pullulans (Ap) on apple leaves in an orchard. We asked three questions. (1) Is variation in fungal population density among leaves caused by variation in leaf carrying capacities and strong density-dependent population growth that maintains densities near carrying capacity? (2) Do resident populations have competitive advantages over immigrant cells? (3) Do Ap dynamics differ at different times during the growing season? To address these questions, we performed two experiments at different times in the growing season. Both experiments used a 2 x 2 factorial design: treatment 1 removed fungal cells from leaves to reveal density-dependent population growth, and treatment 2 inoculated leaves with an Ap strain engineered to express green fluorescent protein (GFP), which made it possible to track the fate of immigrant cells. The experiments showed that natural populations of Ap vary greatly in density due to sustained differences in carrying capacities among leaves. The maintenance of populations close to carrying capacities indicates strong density-dependent processes. Furthermore, resident populations are strongly competitive against immigrants, while immigrants have little impact on residents. Finally, statistical models showed high population growth rates of resident cells in one experiment but not in the other, suggesting that Ap experiences relatively "good" and "bad" periods for population growth. This picture of Ap dynamics conforms to commonly held, but rarely demonstrated, expectations of microbe dynamics in nature. It also highlights the importance of local processes, as opposed to immigration, in determining the abundance and dynamics of microbes on surfaces in terrestrial systems.

Temporal polyethism and worker specialization in the wasp, Vespula germanica.

Temporal polyethism is a common mechanism of worker specialization observed in social insect species with large colony sizes, Vespula wasp colonies consist of thousands of monomorphic workers, yet studies based on small cohorts of workers report that temporal polyethism is either weak or completely absent in different Vespula species. Concerned that the small sample size of these studies precluded detection of temporal polyethism, several hundred, known-age Vespula germanica (F.) (Hymenoptera: Vespidae) workers were studied. High variability was found in the sequence and diversity of tasks workers perform, suggesting that V. germanica colonies exhibit weak temporal polyethism. The most common order in which tasks were taken up was 1) nest work, 2) pulp foraging, 3) carbohydrate foraging, and 4) protein foraging. However, only 61% of the wasps performed more than two of the tasks during their lives. Thorax size had a significant negative effect on the age at first foraging, but the magnitude of the effect was small. The daily ratio of task generalists to specialists was relatively constant despite the high turnover of workers, growth of the colony, and the colony's transition from rearing worker larvae to rearing reproductives. Over the course of their lives, 43% of the workers averaged more than one kind of task performed per day. Life history traits are identified that may explain why vespines with large colonies use a generalist strategy of labor division rather than the specialist strategy observed in honey bees (Apis mellifera) and large colonies of wasps (Polybia occidentalis).

Environmental factors influencing the seasonality of estrus in chimpanzees.

Although the energetics of the estrous cycle in primates is not well understood, evidence suggests that energy and nutrient acquisition influence ovulation and the timing of conception. Energy for estrus has to compete with energy allocated for cellular maintenance, thermoregulation, movement for food, and predation avoidance. While some chimpanzee (Pan troglodytes) populations do not have a seasonal birth period, evidence suggests that there is seasonality in the number of estrous females. Similarly, the onset of postpartum cycles has been reported to be seasonal. We used 33 months of data from the Taï National Park, Côte d'Ivoire, to examine how the number of estrous females in a given month was influenced by the abundance and distribution of food, diet, rainfall and temperature. In a second analysis, we examined if there was a seasonal effect on first estrous swellings in adolescent females and postpartum adult females. Results demonstrated that the number of females in estrous in a given month was positively related to food abundance and percent foraging time spent eating insects, and negatively related to mean rainfall in the two preceding months and the mean high temperature. The timing of first estrous swellings of postpartum females and prepartum young females was positively related to the food abundance, and negatively related to mean high temperature. These results showed that environmental conditions can seasonally limit the energetically demanding estrus cycle. The presence of estrous females increases gregariousness in chimpanzee communities, and this study identified environmental factors that affect estrus directly and hence social grouping indirectly.

Carotid chemoafferent plasticity in adult rats following developmental hyperoxia.

Developmental hyperoxia impairs carotid chemoreceptor development and induces long-lasting reduction in carotid sinus nerve (CSN) responses to hypoxia in adult rats. Studies were carried out to determine if CSN responses to acute hypoxia would exhibit hypoxia-induced plasticity in adult 3-5-months-old rats previously treated with postnatal hyperoxia (60% O2, PNH) of 1, 2, or 4 weeks duration. CSN responses to acute hypoxia were assessed in adult rats exposed to 1 week of sustained hypoxia (12% O2, SH). In normal adult rats and adult rats treated with 1 week of PNH, CSN responses to acute hypoxia were significantly increased in urethane-anesthetized rats when studied 3-5 h after SH. Apparent increases in CSN responses to hypoxia were not significant in rats treated with 2 weeks of PNH and were clearly absent after 4 weeks of PNH, but exponential analysis suggests a PNH duration-dependent plasticity of the CSN response to acute hypoxia after SH. In a second study rats exposed to 2 weeks of PNH were treated with SH for 1 week as adults and acute hypoxic responses were tested 4-5 months later. CSN responses in these rats were unaffected by SH suggesting a lack of persistent SH-induced functional plasticity. We conclude that rats treated with 1 week of PNH retain the capacity for hypoxia-induced plasticity of carotid chemoafferent function and some potential for plasticity may be present after 2 weeks of PNH, whereas 4 weeks of PNH impairs the capability of rats to exhibit plasticity following 1 week of SH.

The synergistic effects of stochasticity and dispersal on population densities.

Using laboratory experiments, simulation models, and analytical techniques, we examined the impact of dispersal on the mean densities of patchily distributed populations. Even when dispersal leads to no net additions or removals of individuals from a population, it may nonetheless increase mean population densities if the net immigration rate is positive when populations are growing and negative when they are declining. As a model system for exploring this phenomenon, we used the yeastlike fungus Aureobasidium pullulans. In a laboratory experiment, we showed that dispersal can both ensure persistence and increase mean population densities even when dispersal among populations causes no direct addition or loss of fungal cells. From the laboratory data, we constructed a plausible model of A. pullulans dynamics among apple leaves within an orchard. This simulation model demonstrated that the effect of dispersal on mean densities is enhanced by three factors: weak density dependence of the dynamics within populations, high environmental variability affecting population growth rates, and lack of synchrony among the fluctuations of populations. Using an analytical model, we showed that the underlying mechanisms for this phenomenon are general, suggesting that a large effect of dispersal on mean population densities is possible in many natural systems.

Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and plant genotype.

This study examined the effects of carbon dioxide (CO2)-, ozone (O3)-, and genotype-mediated changes in quaking aspen (Populus tremuloides) chemistry on performance of the forest tent caterpillar (Malacosoma disstria) and its dipteran parasitoid (Compsilura concinnata) at the Aspen Free-Air CO2 Enrichment (FACE) site. Parasitized and non-parasitized forest tent caterpillars were reared on two aspen genotypes under elevated levels of CO2 and O3, alone and in combination. Foliage was collected for determination of the chemical composition of leaves fed upon by forest tent caterpillars during the period of endoparasitoid larval development. Elevated CO2 decreased nitrogen levels but had no effect on concentrations of carbon-based compounds. In contrast, elevated O3 decreased nitrogen and phenolic glycoside levels, but increased concentrations of starch and condensed tannins. Foliar chemistry also differed between aspen genotypes. CO2, O3, genotype, and their interactions altered forest tent caterpillar performance, and differentially so between sexes. In general, enriched CO2 had little effect on forest tent caterpillar performance under ambient O3, but reduced performance (for insects on one aspen genotype) under elevated O3. Conversely, elevated O3 improved forest tent caterpillar performance under ambient, but not elevated, CO2. Parasitoid larval survivorship decreased under elevated O3, depending upon levels of CO2 and aspen genotype. Additionally, larval performance and masses of mature female parasitoids differed between aspen genotypes. These results suggest that host-parasitoid interactions in forest systems may be altered by atmospheric conditions anticipated for the future, and that the degree of change may be influenced by plant genotype.

Single-leaf resolution of the temporal population dynamics of Aureobasidium pullulans on apple leaves.

The abundance of phylloplane microorganisms typically varies over several orders of magnitude among leaves sampled concurrently. Because the methods traditionally used to sample leaves are destructive, it has remained unclear whether this high variability is due to fixed differences in habitat quality among leaves or to asynchronous temporal variation in the microbial population density on individual leaves. We developed a novel semidestructive assay to repeatedly sample the same apple leaves from orchard trees over time by removing progressively more proximal approximately 1-cm-wide transverse segments. Aureobasidium pullulans densities were determined by standard leaf homogenization and plating procedures and were expressed as CFU per square centimeter of segment. The A. pullulans population densities among leaves were lognormally distributed. The variability in A. pullulans population densities among subsections of a given leaf was one-third to one-ninth the variability among whole leaves harvested concurrently. Sequential harvesting of leaf segments did not result in detectable changes in A. pullulans density on residual leaf surfaces. These findings implied that we could infer whole-leaf A. pullulans densities over time by using partial leaves. When this successive sampling regimen was applied over the course of multiple 7- to 8-day experiments, the among-leaf effects were virtually always the predominant source of variance in A. pullulans density estimates. Changes in A. pullulans density tended to be synchronous among leaves, such that the rank order of leaves arrayed with respect to A. pullulans density was largely maintained through time. Occasional periods of asynchrony were observed, but idiosyncratic changes in A. pullulans density did not contribute appreciably to variation in the distribution of populations among leaves. This suggests that persistent differences in habitat (leaf) quality are primarily responsible for the variation in A. pullulans density among leaves in nature.

Optimal spline smoothing of fMRI time series by generalized cross-validation.

Linear parametric regression models of fMRI time series have correlated residuals. One approach to address this problem is to condition the autocorrelation structure by temporal smoothing. Smoothing splines with the degree of smoothing selected by generalized cross-validation (GCV-spline) provide a method to find an optimal smoother for an fMRI time series. The purpose of this study was to determine if GCV-spline of fMRI time series yields unbiased variance estimates of linear regression model parameters. GCV-spline was evaluated with a real fMRI data set and bias of the variance estimator was computed for simulated time series with autocorrelation structures derived from fMRI data. This study only considered fMRI experimental designs of boxcar type. The results from the real data suggest that GCV-spline determines appropriate amounts of smoothing. The simulations show that the variance estimates are, on average, unbiased. The unbiased variance estimates come at some cost to signal detection efficiency. This study demonstrates that GCV-spline is an appropriate method for smoothing fMRI time series.

Juvenile pubic symphysiodesis in dysplastic puppies at 15 and 20 weeks of age.

OBJECTIVE: To examine the effects of juvenile pubic symphysiodesis (JPS) on hip joint conformation, hip laxity, gait, and the development of degenerative joint disease (DJD) in dysplastic puppies operated at 15 and 20 weeks of age. STUDY DESIGN: Randomized controlled prospective study. ANIMALS-Eighteen female hound puppies with increased hip laxity. METHODS: Puppies were randomized to 1 of 4 treatment groups: JPS at 15 weeks of age (n = 6), sham-operated control at 15 weeks of age (n = 3), JPS at 20 weeks of age (n = 6), and sham-operated control at 20 weeks of age (n = 3). Hip extension with pain scoring, Ortolani palpation, hip reduction angle measurement (HRA), PennHIP radiography (University of Pennsylvania) with measurement of distraction index, Norberg angle measurement, and transverse computed tomographic imaging to measure acetabular angle (AA) and dorsal acetabular rim angle (DARA), were tested preoperatively, and at 1 and 2 years of age. RESULTS: JPS resulted in significant changes in AA, HRA, DARA, and conversion to Ortolani negative status. Larger and more rapid changes in hip conformation were seen when surgery was performed at 15 weeks of age. No significant changes were identified in control dogs. Twenty-five percent of JPS dogs developed DJD whereas 83% of control dogs developed DJD. CONCLUSIONS: JPS resulted in significant improvements in hip joint conformation and hip laxity in dysplastic puppies treated at 15 and 20 weeks of age. Improvements in conformation were significantly greater when surgery was performed at 15 weeks of age. CLINICAL RELEVANCE: JPS appears to be a promising treatment for hip dysplasia and is a safe and technically simple procedure to perform.

Population biology of Aureobasidium pullulans on apple leaf surfaces.

Colonization of apple leaves by the yeast-like fungus Aureobasidium pullulans was studied in the field on eight dates over 2 years. Population densities from adaxial leaf surfaces were approximately log10 0.5-2.6 U higher when enumerated directly along line transects as microscopic counts of A. pullulans cells specifically identified by fluorescence in situ hybridization (FISH) than indirectly as CFU obtained by plating leaf washings from comparable surfaces onto nutrient media. Site-specific mapping of the leaf landscape colonized by A. pullulans was facilitated by use of geographic information system (GIS) software. Colonization was plotted and analyzed both qualitatively (as occupancy) and quantitatively (as density). Overall, when expressed as mean occupancy per date, 22-42% of the microscope fields (each 0.196 mm2) contained > or = 1 A. pullulans cell. Occupancy on a microscope field basis was greater over the midvein (47-89%) or smaller veins (49-65%) than over interveinal regions (11-21%). Intensity of colonization, whether expressed as percentage of total A. pullulans cells associated with a particular leaf feature or as cell density per unit area, was also significantly greater (P < 0.05) over the veinal areas compared with the interveinal areas. The primary fungal morphotypes involved in colonization were blastospores, swollen cells, and chlamydospores; only infrequently were hyphae or pseudohyphae seen. Numbers of microcolonies (> or = 10 clustered cells) and percentage of total A. pullulans cells that occurred as microcolonies increased over the growing season and were significantly greater (P < 0.05) over veinal regions compared with interveinal regions. Locally high concentrations of A. pullulans were associated with naturally occurring micro-wounds in interveinal areas. We conclude that A. pullulans colonizes the phylloplane predominantly as single cells and groups thereof in a highly heterogeneous fashion and that sites exist that are relatively conducive (veins; wounds) or nonconducive (unwounded interveinal areas) for epiphytic fungal growth.

How many choices can your test animal compare effectively? Evaluating a critical assumption of behavioral preference tests.

Behavioral choice tests comprise one of the most commonly used experimental designs in ecology. However a critical assumption of these assays, that the outcome is independent of the number of choices, has not been tested explicitly. We developed a methodology for testing this assumption, and discuss how it can be incorporated into experimental design. The model with which we performed this test consisted of an insect herbivore, the gypsy moth Lymantria dispar L., feeding on a clonal host plant, Populus. We established a dose-response feeding gradient by amending leaves of a single age class with defined concentrations of a diterpene, isopimaric acid, that exhibits feeding deterrent properties. We selected various concentrations that elicited different levels of feeding for subsequent tests in which we modified the number of choices. A sample size of 30 assay units per test generated statistically significant separations in two-way choice tests, yielded statistically significant but somewhat inconsistent results when four concentrations were offered, and failed to provide complete separation when five concentrations were offered. Other factors associated with the number of choices that affected results included specific combinations of doses, physical arrangement of choices, and total consumption per assay unit. We used our results to develop procedures for estimating the sample sizes needed to compare a specified number of choices. We based these methods on power considerations, the requirements for data transformation and inclusion of covariates. We develop a general approach for estimating the number of replicates needed to support a particular number of choices for a test organism, and discuss factors to be considered when relating this approach to various types of behavioral choice assays.

Genotypic variation in response of quaking aspen (Populus tremuloides) to atmospheric CO2 enrichment.

Enriched atmospheric CO2 alters the quantity and quality of plant production, but how such effects vary among plant genotypes is poorly known. We evaluated the independent and interactive effects of CO2 and nutrient availability on growth, allocation and phytochemistry of six aspen (Populus tremuloides Michx.) genotypes. One-year-old trees, propagated from root cuttings, were grown in CO2-controlled glasshouses for 64 days, then harvested. Foliage was analyzed for levels of water, nitrogen, starch, phenolic glycosides and condensed tannins. Of seven plant growth/allocation variables measured, four (biomass production, stem growth, relative growth rate and root:shoot ratio) exhibited marginally to highly significant CO2 × genotype interactions. CO2 enrichment stimulated growth of some genotypes more than others, and this interaction was itself influenced by soil nutrient availability. In addition, enriched CO2 increased the magnitude of the among-genotype variance for four of the growth/allocation variables. Of six foliar chemical constituents analyzed, CO2-mediated responses of two (the phenolic glycoside tremulacin and condensed tannins) varied among genotypes. Moreover, enriched CO2 increased the magnitude of among-genotype variance for four of the chemical variables. Given the importance of these growth and chemical characteristics to the biological fitness of aspen, this research suggests that projected atmospheric CO2 increases are likely to alter the genetic structures and evolutionary trajectories of aspen populations.

Environmental controls on ground cover species composition and productivity in a boreal black spruce forest.

Boreal black spruce forests typically have a dense ground cover of bryophytes. The two main bryophyte groups in boreal black spruce forests, feathermoss and Sphagnum, have ecophysiological characteristics that influence the biogeochemical cycles of black spruce forests differently. The objective of this study was to examine the environmental controls of ground cover composition and net primary production (NPP) of feathermoss and Sphagnum in a boreal black spruce forest in central Saskatchewan. The fraction of Sphagnum ground cover was positively correlated to canopy photosynthetically active radiation (PAR) transmittance (r 2=0.48, P=0.03), but the fraction of feathermoss ground cover was negatively correlated to canopy PAR transmittance in plots where Sphagnum was present (r 2=0.87, P<0.0001). Sphagnum presence was inversely correlated (P=0.0001) to water table index, defined as water table depth relative to the peat layer, while feathermoss occurred in a wider range of microenvironments. Average NPP for 1998 was more than three times greater for Sphagnum (77 g C m-2 year-1) than feathermoss (24 g C m-2 year-1), but the average bryophyte NPP for 1998 was 25 g C m-2 year-1 because feathermoss was the dominant ground cover. The large, but differing, peat carbon content of Sphagnum- versus feathermoss-dominated boreal forests and peatlands necessitates the need to accurately quantify fraction ground cover. Additional validation of the empirical models between environmental variables and fraction ground cover of bryophytes is necessary, but the reported relationships offer an approach to model carbon dynamics of bryophytes in boreal forests and peatlands.