Wolbachia as populations within individual insects: causes and consequences of density variation in natural populations

The population-level dynamics of maternally transmitted endosymbionts, including reproductive parasites, depends primarily on the fitness effects and transmission fidelity of these infections. Although experimental laboratory studies have shown that within-host endosymbiont density can affect both of these factors, the existence of such effects in natural populations has not yet been documented. Using quantitative PCR, we survey the density of male-killing Wolbachia in natural populations of Drosophila innubila females from the Chiricahua Mountains of Arizona. We find that there is substantial (20 000-fold) variation in Wolbachia density among wild flies and that within-host Wolbachia density is positively correlated with both the efficacy of male killing and maternal transmission fidelity. Mean Wolbachia density increases three- to five-fold from early to late in the season. This pattern suggests that Wolbachia density declines with fly age, a conclusion corroborated by a laboratory study of Wolbachia density as a function of age. Finally, we suggest three alternative hypotheses to account for the approximately lognormal distribution of Wolbachia density among wild flies.     

Discriminating tastes: self‐selection of macronutrients in two populations of grasshoppers

Abstract The capacity to self‐select an optimal balance of macronutrients (protein and carbohydrate) is studied in two populations of Melanoplus sanguinipes F. (Orthoptera: Acrididae). One population derives from the subarctic (interior of Alaska) and the other from the temperate zone (Idaho, U.S.A.). Over the duration of the fourth and fifth stadia, Alaskan grasshoppers consistently self‐select a diet centred on a 0.90 ratio of protein : carbohydrate, whereas protein and carbohydrate intake by the Idaho grasshoppers is contingent on the particular food choices presented to them. When restricted to imbalanced diets, the Alaskan grasshoppers develop more rapidly than the Idaho grasshoppers, regardless of diet composition. The Idaho grasshoppers also have a greater amount of lipid than the Alaskan grasshoppers across all diets. Performance measures (body mass, survival, developmental times) are more sensitive to dietary imbalances in the Alaskan grasshoppers than in the Idaho grasshoppers. When fed diets with low, but balanced, proportions of protein and carbohydrate, grasshoppers of both populations are able to increase consumption to compensate for the low concentration of nutrients. The results suggest that demographic responses of insects to changes in host plant quality, such as may result from climate change, may differ among populations within a species.     

Effective size of density‐dependent two‐sex populations: the effect of mating systems

Density dependence in vital rates is a key feature affecting temporal fluctuations of natural populations. This has important implications for the rate of random genetic drift. Mating systems also greatly affect effective population sizes, but knowledge of how mating system and density regulation interact to affect random genetic drift is poor. Using theoretical models and simulations, we compare N_e in short‐lived, density‐dependent animal populations with different mating systems. We study the impact of a fluctuating, density‐dependent sex ratio and consider both a stable and a fluctuating environment. We find a negative relationship between annual N_e/N and adult population size N due to density dependence, suggesting that loss of genetic variation is reduced at small densities. The magnitude of this decrease was affected by mating system and life history. A male‐biased, density‐dependent sex ratio reduces the rate of genetic drift compared to an equal, density‐independent sex ratio, but a stochastic change towards male bias reduces the N_e/N ratio. Environmental stochasticity amplifies temporal fluctuations in population size and is thus vital to consider in estimation of effective population sizes over longer time periods. Our results on the reduced loss of genetic variation at small densities, particularly in polygamous populations, indicate that density regulation may facilitate adaptive evolution at small population sizes.     

Variance within homogeneous phytoplankton populations, III: Analysis of natural populations

A theoretical framework for interpreting flow cytometric histograms from homogeneous phytoplankton populations was developed in part I of this series of articles and applied to chlorophyll fluorescence histograms from clonal cultures in part II. In this paper, we demonstrate the application of this framework to the analysis of cell volume distributions found in a natural assemblage of phytoplankton from the Gulf of California. Flow cytometric analyses of a surface water sample incubated for a period of 61 h revealed the sequential growth and decline of three distinct subpopulations. Cell volume distributions for each subpopulation measured at different times were analyzed, and the theoretical density function described in parts I and II was fitted to these distributions. The range of cell volumes within each subpopulation was similar to that predicted for asynchronous populations.     

Density dependence in blowfly populations: experimental evaluation of non‐parametric time‐series modelling

Two approaches for describing density dependence in demographic rates of stage‐structured populations are compared in this study. Time‐series data from laboratory blowfly populations (Lucilia sericata) have been analysed in a separate study, with a statistical modelling approach that incorporated density dependences as unspecified (non‐parametric) functions. In this study, we assessed density‐dependent structures by manipulating densities of larvae and adults in cohorts of blowflies and measuring the demographic rates. We here compare the density‐dependent structures revealed by the cohort experiments with those estimated by the non‐parametric model. This model estimates the demographic rates to have the following density‐dependent structures: (i) larval survival was non‐linearly density‐dependent (a ‘humped’ function), (ii) adult survival was density‐independent, and (iii) reproductive rate decreased with adult density. In the cohort experiments reported here, (i) juvenile survival exhibited a positive density dependence in low densities (facilitation), which became negative at higher densities (competition). Pupal and adult size decreased with initial larval density. (ii) Adult survival was reduced by high initial larval density, but it was independent of adult density. (iii) Reproductive rate was reduced by high initial larval density, and by high adult density in populations of large individuals (from low larval density). Hence, the results from these experiments support the non‐parametric model estimates regarding density‐dependent structures of demographic rates in the blowfly populations. The mean demographic rates, however, were apparently underestimated by the model. We conclude that non‐parametric modelling is a useful first approach for exploratory analysis of ecological time‐series data.     

‘Big data’ from shrinking pathogen populations

Falling costs for genome sequencing and genotyping mean that population genomic data sets are becoming commonplace for a wide variety of species. Once these data are used for the initial tasks of investigating population structure and demographic history, however, is there reason to go back for more? In this issue of Molecular Ecology, Nkhoma et al. (2013) explore the applications of longitudinal genomic diversity data for detecting changes in the prevalence and transmission of the Plasmodium falciparum malaria parasite in South‐East Asia. While this study finds several genetic signatures indicative of reduced disease transmission, other measures, such as short‐term effective population size, geographical population structure and heterozygosity, were not informative. These results indicate the potential contribution of genomic data to the surveillance of small, dynamic populations, whether they are at risk of extinction or targeted for elimination. The interpretation of such data will require close consideration of biological context, however, at both the species and the population level.     

Diet–demography relationships in a long‐lived predator: from territories to populations

Understanding the mechanisms that shape animal population dynamics is of fundamental interest in ecology, evolution and conservation biology. Food supply is an important limiting factor in most animal populations and may have demographic consequences. Optimal foraging theory predicts greater consumption of preferred prey and less diet diversity when food is abundant, which may benefit key fitness parameters such as productivity and survival. Nevertheless, the correspondence between individual resource use and demographic processes in populations of avian predators inhabiting large geographic areas remains largely unexplored, particularly in complex ecosystems such as those of the Mediterranean basin. Based on a long‐term monitoring program of the diet and demography of Bonelli's eagle Aquila fasciata in western Europe, here we test the hypothesis that a predator's diet is correlated to its breeding productivity and survival at both the territorial and population levels, and ultimately to its population growth rate. At the territorial level, we found that productivity increased with greater consumption of European rabbits Oryctolagus cuniculus, the Bonelli's eagle's preferred prey, and pigeons, an important alternative prey for this predator. The survival of territorial pairs was negatively affected by higher diet diversity, which probably reflected the inability to find sufficient high quality prey. Diet effects at the population level were similar but more noticeable than at the territorial level, i.e. a greater consumption of rabbits, together with lesser consumption of small‐to‐medium avian species (‘other birds’; non‐preferred prey), increased productivity, while greater diet diversity and lower consumption of rabbits was associated with reduced survival and population growth rate. Overall, our study illustrates how the diet of a predator species can be closely related to key individual vital rates, which, in turn, leave a measurable fingerprint on population dynamics within and among populations across large spatial scales.     

Variable populations within variable populations: quantifying mitochondrial heteroplasmy in natural populations of the gynodioecious plant Silene vulgaris

Populations of mitochondria reside within individuals. Among angiosperms, these populations are rarely considered as genetically variable entities and typically are not found to be heteroplasmic in nature, leading to the widespread assumption that plant mitochondrial populations are homoplasmic. However, empirical studies of mitochondrial variation in angiosperms are relatively uncommon due to a paucity of sequence variation. Recent greenhouse studies of Silene vulgaris suggested that heteroplasmy might occur in this species at a level that it is biologically relevant. Here, we use established qualitative methods and a novel quantitative PCR method to study the intraindividual population genetics of mitochondria across two generations in natural populations of S. vulgaris. We show incidences of heteroplasmy for mitochondrial atpA and patterns of inheritance that are suggestive of more widespread heteroplasmy at both atpA and cox1. Further, our results demonstrate that quantitative levels of mitochondrial variation within individuals are high, constituting 26% of the total in one population. These findings are most consistent with a biparental model of mitochondrial inheritance. However, selection within individuals may be instrumental in the maintenance of variation because S. vulgaris is gynodioecious. Male sterility is, in part, regulated by the mitochondrial genome, and strong selection pressures appear to influence the frequency of females in these populations.     

Unpedigreed populations and worst‐case scenarios

A population in which parentage information is not recorded is considered a pedigree “black hole” in terms of genetic management. Integration of animals from such an unpedigreed population into a genetically managed population is often accomplished by assuming a worst‐case scenario and recording all animals as highly interrelated (e.g., full siblings). The assumption that a worst‐case scenario is appropriate under a wide variety of circumstances is evaluated. It was determined that the genetic costs of overestimating relationships among animals from an unpedigreed population are always greater than the genetic costs of underestimating relationships by the same amount. This demonstrates that worst‐case scenarios, which are by definition intentional overestimates, are not generally appropriate. A method of obtaining an estimate that will yield the lowest overall genetic cost using the possible maximum and minimum levels of relatedness among animals from the unpedigreed population is presented along with two methods for implementation. Finally, for cases in which the estimated average relatedness among animals from an unpedigreed population is low, it is recommended that different analytical studbook datasets be used for calculation of inbreeding coefficients and mean kinship coefficients. This strategy would allow close estimation of average relatedness without risking inadvertent pairing of highly related animals from the unpedigreed population. Zoo Biol 20:305–314, 2001. © 2001 Wiley‐Liss, Inc.     

Age‐specific fecundity of mammalian populations: A test of three mathematical models

Empirical age‐specific fecundity distributions are often based on small samples and hence include high levels of sampling error, particularly at the older ages. One solution to this problem is to smooth the distributions using appropriate models. The aim of this article is to compare the utility of three models for smoothing and/or graduating these distributions. The three models examined are 1) the Gamma distribution, 2) the Hadwiger function, and 3) the Brass polynomial. Test data sets consist of four types of primates (including humans), Asian elephants, and Przewalski’s horse (an extinct species). The results indicate that all three models work well with a variety of mammalian data. The simplest of these models, the Brass polynomial, cannot be rejected based on available data and appears to be the optimum choice. Zoo Biol 20:487–499, 2001. © 2002 Wiley‐Liss, Inc.     

Phenotypic plasticity and contemporary evolution in introduced populations: evidence from translocated populations of white sands pupfish (<Emphasis Type="Italic">Cyrpinodon tularosa</Emphasis>)

Contemporary evolution has been shown in a few studies to be an important component of colonization ability, but seldom have researchers considered whether phenotypic plasticity facilitates directional evolution from the invasion event. In the current study, we evaluated body shape divergence of the New Mexico State-threatened White Sands pupfish (Cyprinodon tularosa) that were introduced to brackish, lacustrine habitats at two different time in the recent past (approximately 30 years and 1 year previously) from the same source population (saline river environment). Pupfish body shape is correlated with environmental salinity: fish from saline habitats are characterized by slender body shapes, whereas fish from fresher, yet brackish springs are deep-bodied. In this study, lacustrine populations consisted of an approximately 30-year old population and several 1-year old populations, all introduced from the same source. The body shape divergence of the 30-year old population was significant and greater than any of the divergences of the 1-year old populations (which were for the most part not significant). Nonetheless, all body shape changes exhibited body deepening in less saline environments. We conclude that phenotypic plasticity potentially facilitates directional evolution of body deepening for introduced pupfish populations.     

Activity of disaccharidases in arctic populations: evolutionary aspects disaccharidases in arctic populations

Disorders of dietary sugar assimilation occur more often among native people of the Arctic then in temperate climate inhabitants.It is hypothesized that the limited variety of natural exogenous sugars in the Arctic, and their low content in the traditional diets of native northerners in accordance with a "protein-lipid" type of metabolism weakened selection, favoring diversity of disaccharidase enzymes.     

Ashes to ashes: Intense fires extinguish populations of urban short‐range endemics

Native bushland fragmented by urbanization often experiences increased cover of flammable weeds, reduced biomass turnover and an absence of fuel management combined with increased ignitions. Depending on species’ mobility and dispersal traits, and the extent of burns within urban remnants, such fires may reduce individual survival rates or limit natural recolonization. We monitored the survival of mygalomorph spiders for a year following high‐intensity and low‐intensity fires in Banksia woodland remnants in urban Perth. Of the 257 burrows found, 115 spiders were confirmed to initially survive after intense wildfire, but none were confirmed alive after 12 months. In sharp contrast, only one spider from 103 observed burrows was confirmed dead after a low‐intensity prescribed fire. As there were instances of our monitored mygalomorphs relocating a short distance following only low intensity fires, we also tested whether predation rates were higher in burnt than unburnt areas. Higher rates of predation were found in burnt areas, but this was strongly influenced by both site and predator type. We recommend further consideration of low‐intensity prescribed fire as well as alternative fuel management approaches in urban remnants to better conserve mygalomorph spider populations and other taxa with limited dispersal and/or mobility capabilities.     

Marine stepping‐stones: Connectivity of Mytilus edulis populations between offshore energy installations

Recent papers have suggested that epifaunal organisms use artificial structures as stepping‐stones to spread to areas that are too distant to reach in a single generation. With thousands of artificial structures present in the North Sea, we test the hypothesis that these structures are connected by water currents and act as an interconnected reef. Population genetic structure of the blue mussel, Mytilus edulis, was expected to follow a pattern predicted by a particle tracking model (PTM). Correlation between population genetic differentiation, based on microsatellite markers, and particle exchange was tested. Specimens of M. edulis were found at each location, although the PTM indicated that locations >85 km offshore were isolated from coastal subpopulations. The fixation coefficient F_ST correlated with the number of arrivals in the PTM. However, the number of effective migrants per generation as inferred from coalescent simulations did not show a strong correlation with the arriving particles. Isolation by distance analysis showed no increase in isolation with increasing distance and we did not find clear structure among the populations. The marine stepping‐stone effect is obviously important for the distribution of M. edulis in the North Sea and it may influence ecologically comparable species in a similar way. In the absence of artificial shallow hard substrates, M. edulis would be unlikely to survive in offshore North Sea waters.     

A mother’s legacy: the strength of maternal effects in animal populations

Although mothers influence the traits of their offspring in many ways beyond the transmission of genes, it remains unclear how important such ‘maternal effects’ are to phenotypic differences among individuals. Synthesizing estimates derived from detailed pedigrees, we evaluated the amount of phenotypic variation determined by maternal effects in animal populations. Maternal effects account for half as much phenotypic variation within populations as do additive genetic effects. Maternal effects most greatly affect morphology and phenology but, surprisingly, are not stronger in species with prolonged maternal care than in species without. While maternal effects influence juvenile traits more than adult traits on average, they do not decline across ontogeny for behaviour or physiology, and they do not weaken across the life cycle in species without maternal care. These findings underscore maternal effects as an important source of phenotypic variation and emphasise their potential to affect many ecological and evolutionary processes.     

Genetic diversity of small populations: Not always “doom and gloom”?

Is a key theory of evolutionary and conservation biology—that loss of genetic diversity can be predicted from population size—on shaky ground? In the face of increasing human‐induced species depletion and habitat fragmentation, this question and the study of genetic diversity in small populations are paramount to understanding the limits of species’ responses to environmental change and to providing remedies to endangered species conservation. Few empirical studies have investigated to what degree some small populations might be buffered against losses of genetic diversity. Even fewer studies have experimentally tested the potential underlying mechanisms. The study of Schou, Loeschcke, Bechsgaard, Schlotterer, and Kristensen ( 2017 ) in this issue of Molecular Ecology is elegant in combining classic common garden experimentation with population genomics on an iconic experimental model species (Drosophila melanogaster). The authors reveal a slower rate of loss of genetic diversity in small populations under varying thermal regimes than theoretically expected and hence an unexpected retention of genetic diversity. They are further able to hone in on a plausible mechanism: associative overdominance, wherein homozygosity of deleterious recessive alleles is especially disfavoured in genomic regions of low recombination. These results contribute to a budding literature on the varying mechanisms underlying genetic diversity in small populations and encourage further such research towards the effective management and conservation of fragmented or endangered populations.     

Pop‐Inference: An educational application to evaluate statistical differences among populations

Pop‐Inference is an educational tool designed to help teaching of hypothesis testing using populations. The application allows for the statistical comparison of demographic parameters among populations. Input demographic data are projection matrices or raw demographic data. Randomization tests are used to compare populations. The tests evaluate the hypothesis that demographic parameters differ among groups of individuals more that should be expected from random allocation of individuals to populations. Confidence intervals for demographic parameters are obtained using the bootstrap. Tests may be global or pairwise. In addition to tests on differences, one‐way life table response experiments (LTRE) are available for random and fixed factors. Planned (a priori) comparisons are possible. Power of comparison tests is evaluated by constructing the distribution of the test statistic when the null hypothesis is true and when it is false. The relationship between power and sample size is explored by evaluating differences among populations at increasing population sizes, while keeping vital rates constant.