Congruent Genetic and Demographic Dispersal Rates in a Natural Metapopulation at Equilibrium.

Understanding the functioning of natural metapopulations at relevant spatial and temporal scales is necessary to accurately feed both theoretical eco-evolutionary models and conservation plans. One key metric to describe the dynamics of metapopulations is dispersal rate. It can be estimated with either direct field estimates of individual movements or with indirect molecular methods, but the two approaches do not necessarily match. We present a field study in a large natural metapopulation of the butterfly Boloria eunomia in Belgium surveyed over three generations using synchronized demographic and genetic datasets with the aim to characterize its genetic structure, its dispersal dynamics, and its demographic stability. By comparing the census and effective population sizes, and the estimates of dispersal rates, we found evidence of stability at several levels: constant inter-generational ranking of population sizes without drastic historical changes, stable genetic structure and geographically-influenced dispersal movements. Interestingly, contemporary dispersal estimates matched between direct field and indirect genetic assessments. We discuss the eco-evolutionary mechanisms that could explain the described stability of the metapopulation, and suggest that destabilizing agents like inter-generational fluctuations in population sizes could be controlled by a long adaptive history of the species to its dynamic local environment. We finally propose methodological avenues to further improve the match between demographic and genetic estimates of dispersal.

Genetic costructure in a meta-community under threat of habitat fragmentation.

Habitat fragmentation increasingly threatens the services provided by natural communities and ecosystem worldwide. An understanding of the eco-evolutionary processes underlying fragmentation-compromised communities in natural settings is lacking, yet critical to realistic and sustainable conservation. Through integrating the multivariate genetic, biotic and abiotic facets of a natural community module experiencing various degrees of habitat fragmentation, we provide unique insights into the processes underlying community functioning in real, natural conditions. The focal community module comprises a parasitic butterfly of conservation concern and its two obligatory host species, a plant and an ant. We show that both historical dispersal and ongoing habitat fragmentation shape population genetic diversity of the butterfly Phengaris alcon and its most limited host species (the plant Gentiana pneumonanthe). Genetic structure of each species was strongly driven by geographical structure, altitude and landscape connectivity. Strikingly, however, was the strong degree of genetic costructure among the three species that could not be explained by the spatial variables under study. This finding suggests that factors other than spatial configuration, including co-evolutionary dynamics and shared dispersal pathways, cause parallel genetic structure among interacting species. While the exact contribution of co-evolution and shared dispersal routes on the genetic variation within and among communities deserves further attention, our findings demonstrate a considerable degree of genetic parallelism in natural meta-communities. The significant effect of landscape connectivity on the genetic diversity and structure of the butterfly also suggests that habitat fragmentation may threaten the functioning of the community module on the long run.

Flight Morphology, Compound Eye Structure and Dispersal in the Bog and the Cranberry Fritillary Butterflies: An Inter- and Intraspecific Comparison.

Understanding dispersal is of prime importance in conservation and population biology. Individual traits related to motion and navigation during dispersal may differ: (1) among species differing in habitat distribution, which in turn, may lead to interspecific differences in the potential for and costs of dispersal, (2) among populations of a species that experiences different levels of habitat fragmentation; (3) among individuals differing in their dispersal strategy and (4) between the sexes due to sexual differences in behaviour and dispersal tendencies. In butterflies, the visual system plays a central role in dispersal, but exactly how the visual system is related to dispersal has received far less attention than flight morphology. We studied two butterfly species to explore the relationships between flight and eye morphology, and dispersal. We predicted interspecific, intraspecific and intersexual differences for both flight and eye morphology relative to i) species-specific habitat distribution, ii) variation in dispersal strategy within each species and iii) behavioural differences between sexes. However, we did not investigate for potential population differences. We found: (1) sexual differences that presumably reflect different demands on both male and female visual and flight systems, (2) a higher wing loading (i.e. a proxy for flight performance), larger eyes and larger facet sizes in the frontal and lateral region of the eye (i.e. better navigation capacities) in the species inhabiting naturally fragmented habitat compared to the species inhabiting rather continuous habitat, and (3) larger facets in the frontal region in dispersers compared to residents within a species. Hence, dispersers may have similar locomotory capacity but potentially better navigation capacity. Dispersal ecology and evolution have attracted much attention, but there are still significant gaps in our understanding of the mechanisms of dispersal. Unfortunately, for many species we lack detailed information on the role of behavioural, morphological and physiological traits for dispersal. Our novel study supports the existence of inter- and intra-specific evolutionary responses in both motion and navigation capacities (i.e. flight and eye morphology) linked to dispersal.

Conservation genetics of a threatened butterfly: comparison of allozymes, RAPDs and microsatellites.

BACKGROUND: Addressing genetic issues in the management of fragmented wild populations of threatened species is one of the most important challenges in conservation biology. Nowadays, a diverse array of molecular methods exists to assess genetic diversity and differentiation of wild populations such as allozymes, dominant markers and co-dominant markers. However it remains worthwhile i) to compare the genetic estimates obtained using those several markers in order to ii) test their relative utility, reliability and relevance and iii) the impact of these results for the design of species-specific conservation measures. RESULTS: Following the successful isolation of 15 microsatellites loci for the cranberry fritillary butterfly, Boloria aquilonaris, we analyzed the genetic diversity and structure of eight populations located in four different landscapes, at both the regional and the landscape scales. We confront results based on microsatellites to those obtained using allozymes and RAPDs on the same samples. Genetic population analyses using different molecular markers indicate that the B. aquilonaris populations are characterized by a weak genetic variation, likely due to low effective population size and low dispersal at the regional scale. This results in inbreeding in some populations, which may have detrimental consequences on their long term viability. However, gene flow within landscape is limited but not inexistent, with some long range movements resulting in low or no isolation by distance. Spatial structuring was detected among the most isolated populations. CONCLUSIONS: The use of allozymes and RAPD are of very limited value to determine population structuring at small spatial (i.e. landscape) scales, microsatellites giving much higher estimate resolution. The use of RAPD data is also limited for evidencing inbreeding. However, coarse-grain spatial structure (i.e. regional scale), and gene flow estimates based on RAPD and microsatellites data gave congruent results. At a time with increasing development of new molecular methods and markers, dominant markers may still be worthwhile to consider in organisms for which no genomic information is available, and for which limited resources are available.

A protocol for better design, application, and communication of population viability analyses.

Population viability analyses (PVAs) contribute to conservation theory, policy, and management. Most PVAs focus on single species within a given landscape and address a specific problem. This specificity often is reflected in the organization of published PVA descriptions. Many lack structure, making them difficult to understand, assess, repeat, or use for drawing generalizations across PVA studies. In an assessment comparing published PVAs and existing guidelines, we found that model selection was rarely justified; important parameters remained neglected or their implementation was described vaguely; limited details were given on parameter ranges, sensitivity analysis, and scenarios; and results were often reported too inconsistently to enable repeatability and comparability. Although many guidelines exist on how to design and implement reliable PVAs and standards exist for documenting and communicating ecological models in general, there is a lack of organized guidelines for designing, applying, and communicating PVAs that account for their diversity of structures and contents. To fill this gap, we integrated published guidelines and recommendations for PVA design and application, protocols for documenting ecological models in general and individual-based models in particular, and our collective experience in developing, applying, and reviewing PVAs. We devised a comprehensive protocol for the design, application, and communication of PVAs (DAC-PVA), which has 3 primary elements. The first defines what a useful PVA is; the second element provides a workflow for the design and application of a useful PVA and highlights important aspects that need to be considered during these processes; and the third element focuses on communication of PVAs to ensure clarity, comprehensiveness, repeatability, and comparability. Thereby, DAC-PVA should strengthen the credibility and relevance of PVAs for policy and management, and improve the capacity to generalize PVA findings across studies.

Plant quality and local adaptation undermine relocation in a bog specialist butterfly.

The butterfly Boloria aquilonaris is a specialist of oligotrophic ecosystems. Population viability analysis predicted the species to be stable in Belgium and to collapse in the Netherlands with reduced host plant quality expected to drive species decline in the latter. We tested this hypothesis by rearing B. aquilonaris caterpillars from Belgian and Dutch sites on host plants (the cranberry, Vaccinium oxycoccos). Dutch plant quality was lower than Belgian one conferring lower caterpillar growth rate and survival. Reintroduction and/or supplementation may be necessary to ensure the viability of the species in the Netherlands, but some traits may have been selected solely in Dutch caterpillars to cope with gradual changes in host plant quality. To test this hypothesis, the performance of Belgian and Dutch caterpillars fed with plants from both countries were compared. Dutch caterpillars performed well on both plant qualities, whereas Belgian caterpillars could not switch to lower quality plants. This can be considered as an environmentally induced plastic response of caterpillars and/or a local adaptation to plant quality, which precludes the use of Belgian individuals as a unique solution for strengthening Dutch populations. More generally, these results stress that the relevance of local adaptation in selecting source populations for relocation may be as important as restoring habitat quality.

Should I lay or should I wait? Egg-laying in the two-spotted spider mite Tetranychus urticae Koch.

Optimality theory predicts that females tend to maximize their offspring survival by choosing the egg-laying site. In this context, the use of conspecific cues allows a more reliable assessment of the habitat quality. To test this hypothesis, Tetranychus urticae Koch is an appropriate biological model as it is a phytophagous mite living in group, protected against external aggression by a common web. Experiments were conducted to determine the respective influence of substrate (living substrate: bean leaf vs. non-living substrate: glass plate), silk and presence of conspecific eggs on the egg-laying behavior of T. urticae females. On both living and non-living substrates, the presence of silk positively influenced the probability of a female to lay an egg, but had no influence on the number of eggs deposited. The egg-laying behavior was mainly determined by the nature of the substrate with mites laying fewer eggs on a non-living substrate than on a living one. The presence of a conspecific egg had no impact on either the probability of laying an egg or on the oviposition rate. This study showed a high variability among females in their fecundity and egg-laying performance. The physiology of females (individual fecundity), the egg-laying substrate and to a lesser extent the presence of silk impacted on the decision of spider mites to lay eggs.

Individual dispersal, landscape connectivity and ecological networks.

Connectivity is classically considered an emergent property of landscapes encapsulating individuals' flows across space. However, its operational use requires a precise understanding of why and how organisms disperse. Such movements, and hence landscape connectivity, will obviously vary according to both organism properties and landscape features. We review whether landscape connectivity estimates could gain in both precision and generality by incorporating three fundamental outcomes of dispersal theory. Firstly, dispersal is a multi-causal process; its restriction to an 'escape reaction' to environmental unsuitability is an oversimplification, as dispersing individuals can leave excellent quality habitat patches or stay in poor-quality habitats according to the relative costs and benefits of dispersal and philopatry. Secondly, species, populations and individuals do not always react similarly to those cues that trigger dispersal, which sometimes results in contrasting dispersal strategies. Finally, dispersal is a major component of fitness and is thus under strong selective pressures, which could generate rapid adaptations of dispersal strategies. Such evolutionary responses will entail spatiotemporal variation in landscape connectivity. We thus strongly recommend the use of genetic tools to: (i) assess gene flow intensity and direction among populations in a given landscape; and (ii) accurately estimate landscape features impacting gene flow, and hence landscape connectivity. Such approaches will provide the basic data for planning corridors or stepping stones aiming at (re)connecting local populations of a given species in a given landscape. This strategy is clearly species- and landscape-specific. But we suggest that the ecological network in a given landscape could be designed by stacking up such linkages designed for several species living in different ecosystems. This procedure relies on the use of umbrella species that are representative of other species living in the same ecosystem.

Each life stage matters: the importance of assessing the response to climate change over the complete life cycle in butterflies.

As ectothermic organisms, butterflies have widely been used as models to explore the predicted impacts of climate change. However, most studies explore only one life stage; to our best knowledge, none have integrated the impact of temperature on the vital rates of all life stages for a species of conservation concern. Besides, most population viability analysis models for butterflies are based on yearly population growth rate, precluding the implementation and assessment of important climate change scenarios, where climate change occurs mainly, or differently, during some seasons. Here, we used a combination of laboratory and field experiments to quantify the impact of temperature on all life stages of a vulnerable glacial relict butterfly. Next, we integrated these impacts into an overall population response using a deterministic periodic matrix model and explored the impact of several climate change scenarios. Temperature positively affected egg, pre-diapause larva and pupal survival, and the number of eggs laid by a female; only the survival of overwintering larva was negatively affected by an increase in temperature. Despite the positive impact of warming on many life stages, population viability was reduced under all scenarios, with predictions of much shorter times to extinction than under the baseline (current temperature situation) scenario. Indeed, model predictions were the most sensitive to changes in survival of overwintering larva, the only stage negatively affected by warming. A proper consideration of every stage of the life cycle is important when designing conservation guidelines in the light of climate change. This is in line with the resource-based habitat view, which explicitly refers to the habitat as a collection of resources needed for all life stages of the species. We, therefore, encourage adopting a resource-based habitat view for population viability analysis and development of conservation guidelines for butterflies, and more generally, other organisms. Life stages that are cryptic or difficult to study should not be forsaken as they may be key determinants in the overall response to climate change, as we found with overwintering Boloria eunomia larvae.

Costs of dispersal.

Dispersal costs can be classified into energetic, time, risk and opportunity costs and may be levied directly or deferred during departure, transfer and settlement. They may equally be incurred during life stages before the actual dispersal event through investments in special morphologies. Because costs will eventually determine the performance of dispersing individuals and the evolution of dispersal, we here provide an extensive review on the different cost types that occur during dispersal in a wide array of organisms, ranging from micro-organisms to plants, invertebrates and vertebrates. In general, costs of transfer have been more widely documented in actively dispersing organisms, in contrast to a greater focus on costs during departure and settlement in plants and animals with a passive transfer phase. Costs related to the development of specific dispersal attributes appear to be much more prominent than previously accepted. Because costs induce trade-offs, they give rise to covariation between dispersal and other life-history traits at different scales of organismal organisation. The consequences of (i) the presence and magnitude of different costs during different phases of the dispersal process, and (ii) their internal organisation through covariation with other life-history traits, are synthesised with respect to potential consequences for species conservation and the need for development of a new generation of spatial simulation models.

A meta-analysis of dispersal in butterflies.

Dispersal has recently gained much attention because of its crucial role in the conservation and evolution of species facing major environmental changes such as habitat loss and fragmentation, climate change, and their interactions. Butterflies have long been recognized as ideal model systems for the study of dispersal and a huge amount of data on their ability to disperse has been collected under various conditions. However, no single 'best' method seems to exist leading to the co-occurrence of various approaches to study butterfly mobility, and therefore a high heterogeneity among data on dispersal across this group. Accordingly, we here reviewed the knowledge accumulated on dispersal and mobility in butterflies, to detect general patterns. This meta-analysis specifically addressed two questions. Firstly, do the various methods provide a congruent picture of how dispersal ability is distributed across species? Secondly, is dispersal species-specific? Five sources of data were analysed: multisite mark-recapture experiments, genetic studies, experimental assessments, expert opinions, and transect surveys. We accounted for potential biases due to variation in genetic markers, sample sizes, spatial scales or the level of habitat fragmentation. We showed that the various dispersal estimates generally converged, and that the relative dispersal ability of species could reliably be predicted from their relative vagrancy (records of butterflies outside their normal habitat). Expert opinions gave much less reliable estimates of realized dispersal but instead reflected migration propensity of butterflies. Within-species comparisons showed that genetic estimates were relatively invariable, while other dispersal estimates were highly variable. This latter point questions dispersal as a species-specific, invariant trait.