Christopher Hassall

A comparative analysis of the evolution of imperfect mimicry

Although exceptional examples of adaptation are frequently celebrated, some outcomes of natural selection seem far from perfect. For example, many hoverflies (Diptera: Syrphidae) are harmless (Batesian) mimics of stinging Hymenoptera. However, although some hoverfly species are considered excellent mimics, other species bear only a superficial resemblance to their models and it is unclear why this is so. To evaluate hypotheses that have been put forward to explain interspecific variation in the mimetic fidelity of Palearctic Syrphidae we use a comparative approach. We show that the most plausible explanation is that predators impose less selection for mimetic fidelity on smaller hoverfly species because they are less profitable prey items. In particular, our findings, in combination with previous results, allow us to reject several key hypotheses for imperfect mimicry: first, human ratings of mimetic fidelity are positively correlated with both morphometric measures and avian rankings, indicating that variation in mimetic fidelity is not simply an illusion based on human perception; second, no species of syrphid maps out in multidimensional space as being intermediate in appearance between several different hymenopteran model species, as the multimodel hypothesis requires; and third, we find no evidence for a negative relationship between mimetic fidelity and abundance, which calls into question the kin-selection hypothesis. By contrast, a strong positive relationship between mimetic fidelity and body size supports the relaxed-selection hypothesis, suggesting that reduced predation pressure on less profitable prey species limits the selection for mimetic perfection.

Field estimates of reproductive success in a model insect: behavioural surrogates are poor predictors of fitness

Understanding, and therefore measuring, factors that determine fitness is a central problem in evolutionary biology. We studied a natural population of Coenagrion puella (Odonata: Zygoptera) over two entire breeding seasons, with over a thousand individuals uniquely marked and genotyped, and all mating events at the rendezvous site recorded. Using a parentage analysis, fitness of individuals in the first generation was quantified as the numbers of offspring that survived to maturity. Although mating behaviour can be predicted by environmental and demographical variables, the numbers of mature offspring produced (fitness) cannot, and crucially, are poorly correlated with behavioural observations of mating. While fitness of both sexes was positively related to mating behaviour and to females ectoparasite burden, these behavioural observations explained little more variance in offspring production than environmental and demographical variables. Thus, we demonstrate that behavioural measures of reproductive success are not necessarily reliable estimates of fitness in natural populations.

Disruptive camouflage impairs object recognition

Whether hiding from predators, or avoiding battlefield casualties, camouflage is widely employed to prevent detection. Disruptive coloration is a seemingly well-known camouflage mechanism proposed to function by breaking up an objects salient features (for example their characteristic outline), rendering objects more difficult to recognize. However, while a wide range of animals are thought to evade detection using disruptive patterns, there is no direct experimental evidence that disruptive coloration impairs recognition. Using humans searching for computer-generated moth targets, we demonstrate that the number of edge-intersecting patches on a target reduces the likelihood of it being detected, even at the expense of reduced background matching. Crucially, eye-tracking data show that targets with more edge-intersecting patches were looked at for longer periods prior to attack, and passed-over more frequently during search tasks. We therefore show directly that edge patches enhance survivorship by impairing recognition, confirming that disruptive coloration is a distinct camouflage strategy, not simply an artefact of background matching.

Empirical evidence of senescence in adult damselflies (Odonata: Zygoptera).

1. Age-dependent increases in mortality have been documented in a variety of species of insect under laboratory conditions. However, while strong statistical evidence has been presented for senescence in vertebrate populations in the wild, we know little about the rate and shape of senescence in wild populations of insects. 2. Odonates (damselflies and dragonflies) provide excellent candidate species for evaluating demographic senescence as they are large enough to be marked individually and they are easily re-sighted without recapture. The prevailing opinion - based entirely on qualitative examination of the declines in log numbers alive with time since marking - is that odonates exhibit age-independent daily survivorship. 3. Here, we examine mark-recapture data on the Azure Damselfly Coenagrion puella over two consecutive seasons. For the first time, we evaluate and compare the fit of quantitative models that not only account for weather-dependent daily variation in daily re-sighting rates, but also age-dependent variation in daily survivorship. 4. Models with age-dependent declines in daily survivorship provide a more parsimonious explanation for the data than similar models without these age-dependent effects. In general, models in which mortality increases in an exponential (Gompertz) fashion explain the mark-recapture sequences more efficiently than a range of alternative models, including those in which mortality increases as a power function (Weibull) or reaches a plateau (logistic). These results are indicative of a general senescent decline in physiological functioning, which is particularly marked after 15 days as a mature adult. 5. Weather (temperature, sun and precipitation) and initial mite load influenced the probability of daily re-sighting. Weather and mite load also influenced daily survivorship, but their effects differed between seasons. 6. Overall, fitting models with age as an explicit covariate demonstrates that odonates do indeed senesce. This contradicts previously held assumptions that Odonata do not exhibit age-dependent survivorship in the wild.

Bergmann's rule is maintained during a rapid range expansion in a damselfly

Climate-induced range shifts result in the movement of a sample of genotypes from source populations to new regions. The phenotypic consequences of those shifts depend upon the sample characteristics of the dispersive genotypes, which may act to either constrain or promote phenotypic divergence, and the degree to which plasticity influences the genotype-environment interaction. We sampled populations of the damselfly Erythromma viridulum from northern Europe to quantify the phenotypic (latitude-body size relationship based on seven morphological traits) and genetic (variation at microsatellite loci) patterns that occur during a range expansion itself. We find a weak spatial genetic structure that is indicative of high gene flow during a rapid range expansion. Despite the potentially homogenizing effect of high gene flow, however, there is extensive phenotypic variation among samples along the invasion route that manifests as a strong, positive correlation between latitude and body size consistent with Bergmanns rule. This positive correlation cannot be explained by variation in the length of larval development (voltinism). While the adaptive significance of latitudinal variation in body size remains obscure, geographical patterns in body size in odonates are apparently underpinned by phenotypic plasticity and this permits a response to one or more environmental correlates of latitude during a range expansion.

Study design and mark-recapture estimates of dispersal: A case study with the endangered damselfly Coenagrion mercuriale

Accurate data on dispersal ability are vital to the understanding of how species are affected by fragmented landscapes. However, three factors may limit the ability of field studies to detect a representative sample of dispersal events: (1) the number of individuals monitored, (2) the area over which the study is conducted and (3) the time over which the study is conducted. Using sub-sampling of mark-release-recapture data from a study on the endangered damselfly Coenagrion mercuriale (Charpentier), we show that maximum dispersal distance is strongly related to the number of recaptured individuals in the mark-release-recapture study and the length of time over which the study is conducted. Median dispersal distance is only related significantly to the length of the study. Spatial extent is not associated with either dispersal measure in our analysis. Previously consideration has been given to the spatial scale of dispersal experiments but we demonstrated conclusively that temporal scale and the number of marked individuals also have the potential to affect the measurement of dispersal. Based on quadratic relationships between the maximum dispersal distance, recapture number and length of study, we conclude that a previous study was of sufficient scale to characterise the dispersal kernel of C. mercuriale. Our method of analysis could be used to ensure that the results of mark-release-recapture studies are independent of levels of spatial and temporal investment. Improved confidence in dispersal estimates will enable better management decisions to be made for endangered species.

Predicting the distributions of under-recorded Odonata using species distribution models

1. Absences in distributional data may result either from the true absence of a species or from a false absence due to lack of recording effort. I use general linear models (GLMs) and species distribution models (SDMs) to investigate this problem in North American Odonata and present a potential solution.

Temporal dynamics of aquatic communities and implications for pond conservation

Conservation through the protection of particular habitats is predicated on the assumption that the conservation value of those habitats is stable. We test this assumption for ponds by investigating temporal variation in macroinvertebrate and macrophyte communities over a 10-year period in northwest England. We surveyed 51 ponds in northern England in 1995/6 and again in 2006, identifying all macrophytes (167 species) and all macroinvertebrates (221 species, excluding Diptera) to species. The alpha-diversity, beta-diversity and conservation value of these ponds were compared between surveys. We find that invertebrate species richness increased from an average of 29.5 species to 39.8 species between surveys. Invertebrate gamma-diversity also increased between the two surveys from 181 species to 201 species. However, this increase in diversity was accompanied by a decrease in beta-diversity. Plant alpha-, beta- and gamma-diversity remained approximately constant between the two periods. However, increased proportions of grass species and a complete loss of charophytes suggests that the communities are undergoing succession. Conservation value was not correlated between sampling periods in either plants or invertebrates. This was confirmed by comparing ponds that had been disturbed with those that had no history of disturbance to demonstrate that levels of correlation between surveys were approximately equal in each group of ponds. This study has three important conservation implications: (i) a pond with high diversity or high conservation value may not remain that way and so it is unwise to base pond conservation measures upon protecting currently-speciose habitats; (ii) maximising pond gamma-diversity requires a combination of late and early succession ponds, especially for invertebrates; and (iii) invertebrate and plant communities in ponds may require different management strategies if succession occurs at varying rates in the two groups.

Mean Annual Precipitation Explains Spatiotemporal Patterns of Cenozoic Mammal Beta Diversity and Latitudinal Diversity Gradients in North America

Spatial diversity patterns are thought to be driven by climate-mediated processes. However, temporal patterns of community composition remain poorly studied. We provide two complementary analyses of North American mammal diversity, using (i) a paleontological dataset (2077 localities with 2493 taxon occurrences) spanning 21 discrete subdivisions of the Cenozoic based on North American Land Mammal Ages (36 Ma – present), and (ii) climate space model predictions for 744 extant mammals under eight scenarios of future climate change. Spatial variation in fossil mammal community structure (β diversity) is highest at intermediate values of continental mean annual precipitation (MAP) estimated from paleosols (∼450 mm/year) and declines under both wetter and drier conditions, reflecting diversity patterns of modern mammals. Latitudinal gradients in community change (latitudinal turnover gradients, aka LTGs) increase in strength through the Cenozoic, but also show a cyclical pattern that is significantly explained by MAP. In general, LTGs are weakest when continental MAP is highest, similar to modern tropical ecosystems in which latitudinal diversity gradients are weak or undetectable. Projections under modeled climate change show no substantial change in β diversity or LTG strength for North American mammals. Our results suggest that similar climate-mediated mechanisms might drive spatial and temporal patterns of community composition in both fossil and extant mammals. We also provide empirical evidence that the ecological processes on which climate space models are based are insufficient for accurately forecasting long-term mammalian response to anthropogenic climate change and inclusion of historical parameters may be essential.

The impact of climate-induced distributional changes on the validity of biological water quality metrics

We present data on the distributional changes within an order of macroinvertebrates used in biological water quality monitoring. The British Odonata (dragonflies and damselflies) have been shown to be expanding their range northwards and this could potentially affect the use of water quality metrics. The results show that the families of Odonata that are used in monitoring are shifting their ranges poleward and that species richness is increasing through time at most UK latitudes. These past distributional shifts have had negligible effects on water quality indicators. However, variation in Odonata species richness (particularly in species-poor regions) has a significant effect on water quality metrics. We conclude with a brief review of current and predicted responses of aquatic macroinvertebrates to environmental warming and maintain that caution is warranted in the use of such dynamic biological indicators.