Experimental evolution of dispersal: Unifying theory, experiments and natural systems.

Dispersal is a central life history trait that affects the ecological and evolutionary dynamics of populations and communities. The recent use of experimental evolution for the study of dispersal is a promising avenue for demonstrating valuable proofs of concept, bringing insight into alternative dispersal strategies and trade-offs, and testing the repeatability of evolutionary outcomes. Practical constraints restrict experimental evolution studies of dispersal to a set of typically small, short-lived organisms reared in artificial laboratory conditions. Here, we argue that despite these restrictions, inferences from these studies can reinforce links between theoretical predictions and empirical observations and advance our understanding of the eco-evolutionary consequences of dispersal. We illustrate how applying an integrative framework of theory, experimental evolution and natural systems can improve our understanding of dispersal evolution under more complex and realistic biological scenarios, such as the role of biotic interactions and complex dispersal syndromes.

Shifts in timing and duration of breeding for 73 boreal bird species over four decades.

Breeding timed to match optimal resource abundance is vital for the successful reproduction of species, and breeding is therefore sensitive to environmental cues. As the timing of breeding shifts with a changing climate, this may not only affect the onset of breeding but also its termination, and thus the length of the breeding period. We use an extensive dataset of over 820K nesting records of 73 bird species across the boreal region in Finland to probe for changes in the beginning, end, and duration of the breeding period over four decades (1975 to 2017). We uncover a general advance of breeding with a strong phylogenetic signal but no systematic variation over space. Additionally, 31% of species contracted their breeding period in at least one bioclimatic zone, as the end of the breeding period advanced more than the beginning. We did not detect a statistical difference in phenological responses of species with combinations of different migratory strategy or number of broods. Nonetheless, we find systematic differences in species responses, as the contraction in the breeding period was found almost exclusively in resident and short-distance migrating species, which generally breed early in the season. Overall, changes in the timing and duration of reproduction may potentially lead to more broods co-occurring in the early breeding season-a critical time for species' reproductive success. Our findings highlight the importance of quantifying phenological change across species and over the entire season to reveal shifts in the community-level distribution of bird reproduction.

Global gene flow releases invasive plants from environmental constraints on genetic diversity.

When plants establish outside their native range, their ability to adapt to the new environment is influenced by both demography and dispersal. However, the relative importance of these two factors is poorly understood. To quantify the influence of demography and dispersal on patterns of genetic diversity underlying adaptation, we used data from a globally distributed demographic research network comprising 35 native and 18 nonnative populations of Plantago lanceolata Species-specific simulation experiments showed that dispersal would dilute demographic influences on genetic diversity at local scales. Populations in the native European range had strong spatial genetic structure associated with geographic distance and precipitation seasonality. In contrast, nonnative populations had weaker spatial genetic structure that was not associated with environmental gradients but with higher within-population genetic diversity. Our findings show that dispersal caused by repeated, long-distance, human-mediated introductions has allowed invasive plant populations to overcome environmental constraints on genetic diversity, even without strong demographic changes. The impact of invasive plants may, therefore, increase with repeated introductions, highlighting the need to constrain future introductions of species even if they already exist in an area.

Effects of environment and genotype on dispersal differ across departure, transfer and settlement in a butterfly metapopulation.

Active dispersal is driven by extrinsic and intrinsic factors at the three stages of departure, transfer and settlement. Most empirical studies capture only one stage of this complex process, and knowledge of how much can be generalized from one stage to another remains unknown. Here we use genetic assignment tests to reconstruct dispersal across 5 years and 232 habitat patches of a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We link individual dispersal events to weather, landscape structure, size and quality of habitat patches, and individual genotype to identify the factors that influence the three stages of dispersal and post-settlement survival. We found that nearly all tested factors strongly affected departure probabilities, but that the same factors explained very little variation in realized dispersal distances. Surprisingly, we found no effect of dispersal distance on post-settlement survival. Rather, survival was influenced by weather conditions, quality of the natal habitat patch, and a strong interaction between genotype and occupancy status of the settled habitat patch, with more mobile genotypes having higher survival as colonists rather than as immigrants. Our work highlights the multi-causality of dispersal and that some dispersal costs can only be understood by considering extrinsic and intrinsic factors and their interaction across the entire dispersal process.

Alternative developmental and transcriptomic responses to host plant water limitation in a butterfly metapopulation.

Predicting how climate change affects biotic interactions poses a challenge. Plant-insect herbivore interactions are particularly sensitive to climate change, as climate-induced changes in plant quality cascade into the performance of insect herbivores. Whereas the immediate survival of herbivore individuals depends on plastic responses to climate change-induced nutritional stress, long-term population persistence via evolutionary adaptation requires genetic variation for these responses. To assess the prospects for population persistence under climate change, it is therefore crucial to characterize response mechanisms to climate change-induced stressors, and quantify their variability in natural populations. Here, we test developmental and transcriptomic responses to water limitation-induced host plant quality change in a Glanville fritillary butterfly (Melitaea cinxia) metapopulation. We combine nuclear magnetic resonance spectroscopy on the plant metabolome, larval developmental assays and an RNA sequencing analysis of the larval transcriptome. We observed that responses to feeding on water-limited plants, in which amino acids and aromatic compounds are enriched, showed marked variation within the metapopulation, with individuals of some families performing better on control and others on water-limited plants. The transcriptomic responses were concordant with the developmental responses: families exhibiting opposite developmental responses also produced opposite transcriptomic responses (e.g. in growth-associated transcripts). The divergent responses in both larval development and transcriptome are associated with differences between families in amino acid catabolism and storage protein production. The results reveal intrapopulation variability in plasticity, suggesting that the Finnish M. cinxia metapopulation harbours potential for buffering against drought-induced changes in host plant quality.

Combining range and phenology shifts offers a winning strategy for boreal Lepidoptera.

Species can adapt to climate change by adjusting in situ or by dispersing to new areas, and these strategies may complement or enhance each other. Here, we investigate temporal shifts in phenology and spatial shifts in northern range boundaries for 289 Lepidoptera species by using long-term data sampled over two decades. While 40% of the species neither advanced phenology nor moved northward, nearly half (45%) used one of the two strategies. The strongest positive population trends were observed for the minority of species (15%) that both advanced flight phenology and shifted their northern range boundaries northward. We show that, for boreal Lepidoptera, a combination of phenology and range shifts is the most viable strategy under a changing climate. Effectively, this may divide species into winners and losers based on their propensity to capitalize on this combination, with potentially large consequences on future community composition.

Multidimensional plasticity in the Glanville fritillary butterfly: larval performance is temperature, host and family specific.

Variation in environmental conditions during development can lead to changes in life-history traits with long-lasting effects. Here, we study how variation in temperature and host plant (i.e. the consequences of potential maternal oviposition choices) affects a suite of life-history traits in pre-diapause larvae of the Glanville fritillary butterfly. We focus on offspring survival, larval growth rates and relative fat reserves, and pay specific attention to intraspecific variation in the responses (G × E × E). Globally, thermal performance and survival curves varied between diets of two host plants, suggesting that host modifies the temperature impact, or vice versa. Additionally, we show that the relative fat content has a host-dependent, discontinuous response to developmental temperature. This implies that a potential switch in resource allocation, from more investment in growth at lower temperatures to storage at higher temperatures, is dependent on the larval diet. Interestingly, a large proportion of the variance in larval performance is explained by differences among families, or interactions with this variable. Finally, we demonstrate that these family-specific responses to the host plant remain largely consistent across thermal environments. Together, the results of our study underscore the importance of paying attention to intraspecific trait variation in the field of evolutionary ecology.

The relative importance of local and regional processes to metapopulation dynamics.

Metapopulation dynamics - patch occupancy, colonization and extinction - are the result of complex processes at both local (e.g. environmental conditions) and regional (e.g. spatial arrangement of habitat patches) scales. A large body of work has focused on habitat patch area and connectivity (area-isolation paradigm). However, these approaches often do not incorporate local environmental conditions or fully address how the spatial arrangement of habitat patches (and resulting connectivity) can influence metapopulation dynamics. Here, we utilize long-term data on a classic metapopulation system - the Glanville fritillary butterfly occupying a set of dry meadows and pastures in the Åland islands - to investigate the relative roles of local environmental conditions, geographic space and connectivity in capturing patch occupancy, colonization and extinction. We defined connectivity using traditional measures as well as graph-theoretic measures of centrality. Using boosted regression tree models, we find roughly comparable model performance among models trained on environmental conditions, geographic space or patch centrality. In models containing all of the covariates, we find strong and consistent evidence for the roles of resource abundance, longitude and centrality (i.e. connectivity) in predicting habitat patch occupancy and colonization, while patch centrality (connectivity) was relatively unimportant for predicting extinction. Relative variable importance did not change when geographic coordinates were not considered and models underwent spatially stratified cross-validation. Together, this suggests that the combination of regional-scale connectivity measures and local-scale environmental conditions is important for predicting metapopulation dynamics and that a stronger integration of ideas from network theory may provide insight into metapopulation processes.

The effect of summer drought on the predictability of local extinctions in a butterfly metapopulation.

The ecological impacts of extreme climatic events on population dynamics and community composition are profound and predominantly negative. Using extensive data of an ecological model system, we tested whether predictions from ecological models remain robust when environmental conditions are outside the bounds of observation. We observed a 10-fold demographic decline of the Glanville fritillary butterfly (Melitaea cinxia) metapopulation on the Åland islands, Finland in the summer of 2018 and used climatic and satellite data to demonstrate that this year was an anomaly with low climatic water balance values and low vegetation productivity indices across Åland. Population growth rates were strongly associated with spatiotemporal variation in climatic water balance. Covariates shown previously to affect the extinction probability of local populations in this metapopulation were less informative when populations were exposed to severe drought during the summer months. Our results highlight the unpredictable responses of natural populations to extreme climatic events.

El Efecto de la Sequía Estival sobre la Previsibilidad de las Extinciones Locales en una Metapoblación de Mariposas Resumen Los impactos ecológicos de los eventos climáticos extremos sobre las dinámicas metapoblacionales y la composición de la comunidad son profundos y predominantemente negativos. Con los extensos datos de un sistema de modelos ecológicos probamos si las predicciones de los modelos ecológicos todavía son sólidos cuando las condiciones ambientales se encuentran fuera de los límites de observación. Observamos una declinación demográfica ocurrir diez veces en la metapoblación de la mariposa Melitaea cinxia en las Islas Aland de Finlandia durante el verano de 2018. Usamos datos climáticos y satelitales para demostrar que ese año fue una anomalía al contar con valores bajos de balance hídrico e índices bajos de productividad de la vegetación en todas las islas. Las tasas de crecimiento poblacional estuvieron fuertemente asociadas con la variación espaciotemporal del balance hídrico climático. Las covarianzas que previamente han afectado a la probabilidad de extinción de las poblaciones locales de esta metapoblación fueron menos informativas cuando las poblaciones estuvieron expuestas a sequías severas durante los meses de verano. Nuestros resultados resaltan las respuestas impredecibles de las poblaciones naturales ante los eventos climáticos extremos.

The microbiome of the Melitaea cinxia butterfly shows marked variation but is only little explained by the traits of the butterfly or its host plant.

Understanding of the ecological factors that shape intraspecific variation of insect microbiota in natural populations is relatively poor. In Lepidopteran caterpillars, microbiota is assumed to be mainly composed of transient bacterial symbionts acquired from the host plant. We sampled Glanville fritillary (Melitaea cinxia) caterpillars from natural populations to describe their gut microbiome and to identify potential ecological factors that determine its structure. Our results demonstrate high variability of microbiota composition even among caterpillars that shared the same host plant individual and most likely the same genetic background. We observed that the caterpillars harboured microbial classes that varied among individuals and alternated between two distinct communities (one composed of mainly Enterobacteriaceae and another with more variable microbiota community). Even though the general structure of the microbiota was not attributed to the measured ecological factors, we found that phylogenetically similar microbiota showed corresponding responses to the sex and the parasitoid infection of the caterpillar and to those of the host plant's microbial and chemical composition. Our results indicate high among-individual variability in the microbiota of the M. cinxia caterpillar and contradict previous findings that the host plant is the major driver of the microbiota communities of insect herbivores.

Metapopulation dynamics in a changing climate: Increasing spatial synchrony in weather conditions drives metapopulation synchrony of a butterfly inhabiting a fragmented landscape.

Habitat fragmentation and climate change are both prominent manifestations of global change, but there is little knowledge on the specific mechanisms of how climate change may modify the effects of habitat fragmentation, for example, by altering dynamics of spatially structured populations. The long-term viability of metapopulations is dependent on independent dynamics of local populations, because it mitigates fluctuations in the size of the metapopulation as a whole. Metapopulation viability will be compromised if climate change increases spatial synchrony in weather conditions associated with population growth rates. We studied a recently reported increase in metapopulation synchrony of the Glanville fritillary butterfly (Melitaea cinxia) in the Finnish archipelago, to see if it could be explained by an increase in synchrony of weather conditions. For this, we used 23 years of butterfly survey data together with monthly weather records for the same period. We first examined the associations between population growth rates within different regions of the metapopulation and weather conditions during different life-history stages of the butterfly. We then examined the association between the trends in the synchrony of the weather conditions and the synchrony of the butterfly metapopulation dynamics. We found that precipitation from spring to late summer are associated with the M. cinxia per capita growth rate, with early summer conditions being most important. We further found that the increase in metapopulation synchrony is paralleled by an increase in the synchrony of weather conditions. Alternative explanations for spatial synchrony, such as increased dispersal or trophic interactions with a specialist parasitoid, did not show paralleled trends and are not supported. The climate driven increase in M. cinxia metapopulation synchrony suggests that climate change can increase extinction risk of spatially structured populations living in fragmented landscapes by altering their dynamics.

Sex-dependent effects of larval food stress on adult performance under semi-natural conditions: only a matter of size?

Organisms with complex life-cycles acquire essential nutrients as juveniles, and hence even a short-term food stress during development can impose serious fitness costs apparent in adults. We used the Glanville fritillary butterfly to investigate the effects of larval food stress on adult performance under semi-natural conditions in a population enclosure. We were specifically interested in whether the negative effects observed were due to body mass reduction only or whether additional effects unrelated to pupal mass were evident. The two sexes responded differently to the larval food stress. In females, larval food stress reduced pupal mass and reproductive performance. The reduced reproductive performance was partially mediated by pupal mass reduction. Food stressed females also had reduced within-patch mobility, and this effect was not dependent on pupal mass. Conversely, food stress had no effect on male pupal mass, suggesting a full compensation via prolonged development time. Nonetheless, food stressed males were less likely to sire any eggs, potentially due to changes in their territorial behavior, as indicated by food stress also increasing male within-patch mobility (i.e., patrolling behavior). When males did sire eggs, the offspring number and viability were unaffected by male food stress treatment. Viability was in general higher for offspring sired by lighter males. Our study highlights how compensatory mechanisms after larval food stress can act in a sex-specific manner and that the alteration in body mass is only partially responsible for the reduced adult performance observed.

Evolutionary adaptation to climate change.

When the notion of climate change emerged over 200 years ago, few speculated as to the impact of rising atmospheric temperatures on biological life. Tens of decades later, research clearly demonstrates that the impact of climate change on life on Earth is enormous, ongoing, and with foreseen effects lasting well into the next century. Responses to climate change have been widely documented. However, the breadth of phenotypic traits involved with evolutionary adaptation to climate change remains unclear. In addition, it is difficult to identify the genetic and/or epigenetic bases of phenotypes adaptive to climate change, in part because it often is not clear whether this change is plastic, genetic, or some combination of the two. Adaptive responses to climate-driven selection also interact with other processes driving genetic changes in general, including demography as well as selection driven by other factors. In this Special Issue, we explore the factors that will impact the overall outcome of climate change adaptation. Our contributions explain that traits involved in climate change adaptation include not only classic phenomena, such as range shifts and environmentally dependent sex determination, but also often overlooked phenomena such as social and sexual conflicts and the expression of stress hormones. We learn how climate-driven selection can be mediated via both natural and sexual selection, effectively influencing key fitness-related traits such as offspring growth and fertility as well as evolutionary potential. Finally, we explore the limits and opportunities for predicting adaptive responses to climate change. This contribution forms the basis of 10 actions that we believe will improve predictions of when and how organisms may adapt genetically to climate change. We anticipate that this Special Issue will inform novel investigations into how the effects of climate change unfold from phenotypes to genotypes, particularly as methodologies increasingly allow researchers to study selection in field experiments.

Recent range shifts of moths, butterflies, and birds are driven by the breadth of their climatic niche.

Species are altering their ranges as a response to climate change, but the magnitude and direction of observed range shifts vary considerably among species. The ability to persist in current areas and colonize new areas plays a crucial role in determining which species will thrive and which decline as climate change progresses. Several studies have sought to identify characteristics, such as morphological and life-history traits, that could explain differences in the capability of species to shift their ranges together with a changing climate. These characteristics have explained variation in range shifts only sporadically, thus offering an uncertain tool for discerning responses among species. As long-term selection to past climates have shaped species' tolerances, metrics describing species' contemporary climatic niches may provide an alternative means for understanding responses to on-going climate change. Species that occur in a broader range of climatic conditions may hold greater tolerance to climatic variability and could therefore more readily maintain their historical ranges, while species with more narrow tolerances may only persist if they are able to shift in space to track their climatic niche. Here, we provide a first-filter test of the effect of climatic niche dimensions on shifts in the leading range edges in three relatively well-dispersing species groups. Based on the realized changes in the northern range edges of 383 moth, butterfly, and bird species across a boreal 1,100 km latitudinal gradient over c. 20 years, we show that while most morphological or life-history traits were not strongly connected with range shifts, moths and birds occupying a narrower thermal niche and butterflies occupying a broader moisture niche across their European distribution show stronger shifts towards the north. Our results indicate that the climatic niche may be important for predicting responses under climate change and as such warrants further investigation of potential mechanistic underpinnings.

When and how can we predict adaptive responses to climate change?

Predicting if, when, and how populations can adapt to climate change constitutes one of the greatest challenges in science today. Here, we build from contributions to the special issue on evolutionary adaptation to climate change, a survey of its authors, and recent literature to explore the limits and opportunities for predicting adaptive responses to climate change. We outline what might be predictable now, in the future, and perhaps never even with our best efforts. More accurate predictions are expected for traits characterized by a well-understood mapping between genotypes and phenotypes and traits experiencing strong, direct selection due to climate change. A meta-analysis revealed an overall moderate trait heritability and evolvability in studies performed under future climate conditions but indicated no significant change between current and future climate conditions, suggesting neither more nor less genetic variation for adapting to future climates. Predicting population persistence and evolutionary rescue remains uncertain, especially for the many species without sufficient ecological data. Still, when polled, authors contributing to this special issue were relatively optimistic about our ability to predict future evolutionary responses to climate change. Predictions will improve as we expand efforts to understand diverse organisms, their ecology, and their adaptive potential. Advancements in functional genomic resources, especially their extension to non-model species and the union of evolutionary experiments and "omics," should also enhance predictions. Although predicting evolutionary responses to climate change remains challenging, even small advances will reduce the substantial uncertainties surrounding future evolutionary responses to climate change.

The predictive adaptive response: modeling the life-history evolution of the butterfly Bicyclus anynana in seasonal environments.

A predictive adaptive response (PAR) is a type of developmental plasticity where the response to an environmental cue is not immediately advantageous but instead is later in life. The PAR is a way for organisms to maximize fitness in varying environments. Insects living in seasonal environments are valuable model systems for testing the existence and form of PAR. Previous manipulations of the larval and the adult environments of the butterfly Bicyclus anynana have shown that individuals that were food restricted during the larval stage coped better with forced flight during the adult stage compared to those with optimal conditions in the larval stage. Here, we describe a state-dependent energy allocation model, which we use to test whether such a response to food restriction could be adaptive in nature where this butterfly exhibits seasonal cycles. The results from the model confirm the responses obtained in our previous experimental work and show how such an outcome was facilitated by resource allocation patterns to the thorax during the pupal stage. We conclude that for B. anynana, early-stage cues can direct development toward a better adapted phenotype later in life and, therefore, that a PAR has evolved in this species.

Temperature treatments during larval development reveal extensive heritable and plastic variation in gene expression and life history traits.

Little is known about variation in gene expression that affects life history traits in wild populations of outcrossing species. Here, we analyse heritability of larval development traits and associated variation in gene expression in the Glanville fritillary butterfly (Melitaea cinxia) across three ecologically relevant temperatures. We studied the development of final-instar larvae, which is greatly affected by temperature, and during which stage larvae build up most of the resources for adult life. Larval development time and weight gain varied significantly among families sampled from hundreds of local populations, indicating substantial heritable variation segregating in the large metapopulation. Global gene expression analysis using common garden-reared F2 families revealed that 42% of the >8000 genes surveyed exhibited significant variation among families, 39% of the genes showed significant variation between the temperature treatments, and 18% showed a significant genotype-by-environment interaction. Genes with large family and temperature effects included larval serum protein and cuticle-binding protein genes, and the expression of these genes was closely correlated with the rate of larval development. Significant expression variation in these same categories of genes has previously been reported among adult butterflies originating from newly established versus old local populations, supporting the notion of a life history syndrome put forward based on ecological studies and involving larval development and adult dispersal capacity. These findings suggest that metapopulation dynamics in heterogeneous environments maintain heritable gene expression variation that affects the regulation of life history traits.

Plastic larval development in a butterfly has complex environmental and genetic causes and consequences for population dynamics.

1. In insects, the length of larval development time typically influences adult body size and individual fitness, and hence development time can be expected to respond in an adaptive manner to variation in environmental conditions. In the wild, larval growth may be influenced by individual condition, which can be affected by population-level parameters such as population density and abundance and quality of resources. 2. We sampled larvae of the Glanville fritillary butterfly (Melitaea cinxia) from 514 local populations across a large metapopulation before the winter diapause and reared the larvae in common garden conditions after diapause. Here, we report that small post-diapause larvae prolonged their development via an extra larval instar, apparently to compensate for their 'bad start' after diapause. The number of instars was additionally a plastic response to environmental conditions, as the frequency of the extra instar increased under cooler thermal conditions. 3. The benefit of the extra instar is clear, as it allows individuals to develop into larger adults, but the cost is delayed adult eclosion, which is likely to select against the extra instar especially in males, in which early eclosion is critical for mating success. In support of this, the frequency of the extra instar was significantly lower in males (7%) than in females (42%). 4. Polymorphisms in three genes, serpin-1, vitellin-degrading protease precursor and phosphoglucose isomerase, which are known to influence development in insects, were associated with the occurrence of the extra instar. 5. At the level of local populations, the frequency of the extra instar was higher in newly established populations than that in old local ones, possibly reflecting maternal effects, as new populations are often established by females with heavy investment in dispersal. The frequency of the extra instar in turn correlated with the change in population size over 1 year and the risk of local extinction in the natural metapopulation of the Glanville fritillary. 6. Our results highlight the importance of the physiological condition of individuals in shaping subsequent life-history events and even population dynamics.

Mixed effects of a national protected area network on terrestrial and freshwater biodiversity.

Protected areas are considered fundamental to counter biodiversity loss. However, evidence for their effectiveness in averting local extinctions remains scarce and taxonomically biased. We employ a robust counterfactual multi-taxon approach to compare occupancy patterns of 638 species, including birds (150), mammals (23), plants (39) and phytoplankton (426) between protected and unprotected sites across four decades in Finland. We find mixed impacts of protected areas, with only a small proportion of species explicitly benefiting from protection-mainly through slower rates of decline inside protected areas. The benefits of protection are enhanced for larger protected areas and are traceable to when the sites were protected, but are mostly unrelated to species conservation status or traits (size, climatic niche and threat status). Our results suggest that the current protected area network can partly contribute to slow down declines in occupancy rates, but alone will not suffice to halt the biodiversity crisis. Efforts aimed at improving coverage, connectivity and management will be key to enhance the effectiveness of protected areas towards bending the curve of biodiversity loss.

Cracking the olfactory code of a butterfly: the scent of ageing.

Although olfaction is a primary mode of communication, its importance in sexual selection remains understudied. Here, using the butterfly Bicyclus anynana, we address all the parameters of importance to sexual selection for a male olfactory signal. We show that variation in the male sex pheromone composition indicates male identity and male age. Courting males of different ages display small absolute (c. 200 ng) but large relative (100%) change of one specific pheromone component (hexadecanal) which, unlike the other components, showed no heritability. Females prefer to mate with mid-aged over younger males and the pheromone composition is sufficient to determine this preference. Surprisingly refined information is thus present in the male olfactory signal and is used for sexual selection. Our data also reveal that there may be no 'lek paradox' to resolve once the precise signal of importance to females is identified, as hexadecanal is, as expected, depleted in additive genetic variation.