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van Bergen, E.

Publications and source records attributed to van Bergen, E..

17 recordsLinked to original sources

Dietary ethanol affects feeding behaviour, flight performance, and mating success in a fruit-feeding butterfly

O_LIThe evolution of fleshy fruits around 124 million years ago introduced a nutritious resource and drove shifts toward fruit-feeding across the animal kingdom, leading to a variety of adaptations for locating and exploiting this resource. Fruits are inherently dynamic, changing in physical, chemical, and biological properties as they progress from development through ripening to decay. C_LIO_LIFruit fermentation produces ethanol, a volatile compound that is simultaneously caloric, intoxicating, and potentially noxious. While the immediate and long-term effects of dietary ethanol are well documented in mammals, and to some extent in insects such as Drosophila, very little is known about its impact on frugivorous butterflies. C_LIO_LIAlthough ethanol can serve as a foraging cue for frugivorous butterflies, its ingestion may impair performance and reduce fitness. Here, we examine how dietary ethanol affects ecologically and reproductively relevant behaviours in the Afrotropical butterfly Bicyclus anynana, a species that feeds on fermenting fruits in the wild. C_LIO_LIWe found that butterflies exposed to ethanol-supplemented diets initiated feeding more rapidly, but also spent less time feeding, and they required more stimuli to sustain flight. Moreover, feeding behaviour differed between males and females and between mated and virgin individuals, while flight performance differed between sexes but was not affected by mating status. C_LIO_LIGiven the involvement of flight in male courtship, we also tested the hypothesis that negative effects of ethanol consumption on flight would impair courtship. We found that males fed on ethanol-supplemented diets--particularly young ones--had reduced mating success and took longer to secure a mating. C_LIO_LITogether, our findings demonstrate that ethanol consumption affects behaviours closely tied to survival and fitness in B. anynana, suggesting that exposure to fermenting resources may impose selective pressures on physiology, behaviour, and reproductive strategies in frugivorous insects. C_LI

animal behavior and cognition↗

Evolutionary constraints in host shifts: limited adaptation of Plutella xylostella to cardenolide-defended Erysimum cheiranthoides

O_LIPlants and herbivorous insects are engaged in long-term coevolutionary arms races, where gains in novel plant defences and corresponding adaptations in herbivores may drive evolutionary change. One such recent innovation is the gain of cardenolide toxins in the Brassicaceae genus Erysimum, which resulted in the effective deterrence of most herbivores by these plants. Nonetheless, some herbivores continue to attack Erysimum, likely by tolerating cardenolide defences through general detoxification mechanisms that may serve as evolutionary stepping-stones for more specialized resistance. C_LIO_LIWe investigated the interaction between diamondback moth (DBM, Plutella xylostella) and its occasional host plant E. cheiranthoides, by first screening the standing variation in DBM performance, and second by experimentally evolving DBM populations for increased performance on Erysimum. Despite considerable variation among wild DBM populations, larvae consistently avoided Erysimum leaves for feeding, and when constrained to Erysimum, they exhibited reduced growth rate, survival, and lower adult size compared to individuals feeding on control broccoli plants. C_LIO_LISurprisingly, cardenolides could only partly explain the reduced performance of DBM on Erysimum, and experimental evolution failed to improve overall performance. Instead, phenotypes of evolved lines converged on what appears to be a pre-existing, highly plastic phenotype found among wild DBM ancestors and which is characterized by rapid development and high weight gain on control plants, but slow development and low weight gain on Erysimum. C_LIO_LIAlthough DBM failed to evolve improved performance on Erysimum, our results demonstrate that its existing genetic variation and phenotypic plasticity are evidently sufficient to support long-term development on Erysimum, thereby fulfilling a key condition for the future evolution of specialized adaptations. C_LI

evolutionary biology↗

Thermal plasticity in protective wing pigmentation is modulated by genotype and food availability in an insect model of seasonal polyphenism.

Developmental plasticity refers to the phenomenon whereby an organisms phenotype depends on the environmental conditions experienced during development. This plasticity can match phenotype to ecological conditions and help organisms to cope with environmental heterogeneity, including differences between alternating seasons. Experimental studies of developmental plasticity often focus on the impact of individual environmental cues and do not take explicit account of genetic variation. In contrast, natural environments are complex, comprising multiple variables with combined effects that are poorly understood and may vary among genotypes. We investigated the effects of multifactorial environments on the development of the seasonally plastic eyespots of Bicyclus anynana butterflies. Eyespot size is known to depend on developmental temperature and to be involved in alternative seasonal strategies for predator avoidance. In nature, both temperature and food availability undergo seasonal fluctuations. However, our understanding of whether thermal plasticity in eyespot size varies in relation to food availability and across genotypes remains limited. To address this, we investigated the combined effects of temperature (T; two levels: 20{degrees}C and 27{degrees}C) and food availability (N; two levels: control and limited) during development. We examined their impact on wing and eyespot size in adult males and females from multiple genotypes (G; 28 families). We found evidence of thermal and nutritional plasticity, and of temperature-by-nutrition interactions (significant TxN) on the size of eyespots in both sexes. Food limitation resulted in relatively smaller eyespots and tempered the effects of temperature. Additionally, we found differences among families for thermal plasticity (significant GxT effects), but not for nutritional plasticity (non-significant GxN effects) nor for the combined effects of temperature and food limitation (non-significant GxTxN effects). Our results reveal the context dependence of thermal plasticity, with the slope of thermal reaction norms varying across genotypes and across nutritional environments. We discuss these results in light of the ecological significance of pigmentation and the value of considering thermal plasticity in studies of the biological impact of climate change.

evolutionary biology↗

Larval growth rate affects wing shape more than eyespot size in the seasonally polyphenic butterfly Melanitis leda

Butterflies often show adaptive phenotypic plasticity where environmental cues during early stages are used to produce a phenotype that maximizes fitness in the environment experienced by adults. Many tropical satyrine butterflies (Nymphalidae: Satyrinae) are seasonally polyphenic and produce distinct wet- and dry-season form adults providing tight environment-phenotype matching in seasonal environments. Dry-season forms, which are expressed in the dry season, can be induced in the laboratory by growing larvae at low temperatures or on poor food quality. Since both these factors also tend to reduce larval growth rate, larval growth rate may be an internal cue that translates the environmental cues into the expression of phenotypes. If this is the case, we predict that slower-growing larvae would be more likely to develop a dry-season phenotype. To test this hypothesis, we measured both larval growth rate and adult phenotype (eyespot size and wing shape) of individuals of the common evening brown butterfly (Melanitis leda), reared at various temperatures and on various host-plant species. We found that among treatments, larvae with lower growth rates (low temperature, particular host plants) were more likely to develop dry-season phenotypes (small eyespots, falcate wing tips), but within treatments, larval growth rate was mainly linked to wing shape, not eyespot size. These relationships tended to be stronger for males than females as males showed a wider range of eyespot sizes and wing shapes. Overall, only plasticity in wing shape appears to be (partly) mediated by larval growth, and in a sex-specific manner.

evolutionary biology↗

Escaping herbivory through chemical novelty? Field performance and herbivore attack of the cardenolide-producing crucifer plant Erysimum cheiranthoides

Plants in the Brassicaceae produce glucosinolates as potent defenses against generalist herbivores, but many specialists can tolerate or deactivate these compounds. As a potential counter-adaptation, plants in the genus Erysimum evolved novel cardenolide defenses alongside ancestral glucosinolates. Here we grew the dually defended E. cheiranthoides and the phenologically similar Rhamnospermum nigrum in agricultural fields surrounded by Brassicaceae crops and monitored herbivore communities, leaf damage, and plant performance of focal plants over two seasons. In the second year, we additionally manipulated herbivore density and plant competition to identify direct and indirect effects on plant fitness. Both plant species were attacked by a diverse community of specialist herbivores, but most herbivores strongly preferred R. nigrum, reaching higher densities and causing intense damage that suppressed growth of these plants. A similar herbivore community attacked dually-defended E. cheiranthoides, but herbivores occurred at lower densities, caused less damage, and had no negative effect on growth. Consequently, herbivore suppression through pesticide application increased R. nigrum growth but provided no benefit to E. cheiranthoides. In fact, for E. cheiranthoides growing under heterospecific competition, pesticide application reduced growth due to increased competition by R. nigrum. Our results agree with a successful escape of E. cheiranthoides from herbivory, as even though plants are still attacked when herbivores are abundant, these herbivores caused little damage and caused no reduction in fitness. However, the escape from herbivory has likely come at loss of competitive ability when herbivore pressure is low, which would explain why despite its key innovation, E. cheiranthoides has been unable to gain dominance in any plant community.

ecology↗

Genetic contributions of noncognitive skills to academic development

Noncognitive skills such as motivation and self-regulation, are partly heritable and predict academic achievement beyond cognitive skills. However, how the relationship between noncognitive skills and academic achievement changes over development is unclear. The current study examined how cognitive and noncognitive skills contribute to academic achievement from ages 7 to 16 in a sample of over 10,000 children from England and Wales. Noncognitive skills were increasingly predictive of academic achievement across development. Twin and polygenic scores analyses found that the contribution of noncognitive genetics to academic achievement became stronger over the school years. Results from within-family analyses indicated that associations with noncognitive genetics could not simply be attributed to confounding by environmental differences between nuclear families and are consistent with a possible role for evocative/active gene-environment correlations. By studying genetic effects through a developmental lens, we provide novel insights into the role of noncognitive skills in academic development.

genetics↗

Multilevel Twin Models: Geographical Region as a Third Level Variable

The classical twin model can be reparametrized as an equivalent multilevel model. The multilevel parameterization has underexplored advantages, such as the possibility to include higher-level clustering variables in which lower levels are nested. When this higher-level clustering is not modeled, its variance is captured by the common environmental variance component. In this paper we illustrate the application of a 3-level multilevel model to twin data by analyzing the regional clustering of 7-year-old childrens height in the Netherlands. Our findings show that 1.8%, of the phenotypic variance in childrens height is attributable to regional clustering, which is 7% of the variance explained by between-family or common environmental components. Since regional clustering may represent ancestry, we also investigate the effect of region after correcting for genetic principal components, in a subsample of participants with genome-wide SNP data. After correction, region did no longer explain variation in height. Our results suggest that the phenotypic variance explained by region actually represent ancestry effects on height.

genetics↗

Improved chromosome level genome assembly of the Glanville fritillary butterfly (Melitaea cinxia) based on SMRT Sequencing and linkage map.

The Glanville fritillary (Melitaea cinxia) butterfly is a long-term model system for metapopulation dynamics research in fragmented landscapes. Here, we provide a chromosome level assembly of the butterflys genome produced from Pacific Biosciences sequencing of a pool of males, combined with a linkage map from population crosses. The final assembly size of 484 Mb is an increase of 94 Mb on the previously published genome. Estimation of the completeness of the genome with BUSCO, indicates that the genome contains 93 - 95% of the BUSCO genes in complete and single copies. We predicted 14,830 gene models using the MAKER pipeline and manually curated 1,232 of these gene models. The genome and its annotated gene models are a valuable resource for future comparative genomics, molecular biology, transcriptome and genetics studies on this species.

genomics↗

Parental influences on offspring education: indirect genetic effects of non-cognitive skills

Understanding how parents cognitive and non-cognitive skills influence offspring education is vital for educational, family and economic policy. We use genetics (GWAS-by-subtraction) to assess a latent, broad non-cognitive skills dimension. To index parental effects controlling for genetic transmission, we estimate indirect parental genetic effects of polygenic scores on childhood and adulthood educational outcomes, using siblings (N=47,459), adoptees (N=6,407), and parent-offspring trios (N=2,534) in three UK and Dutch cohorts. We find that parental cognitive and non-cognitive skills affect offspring education through their environment: on average across cohorts and designs, indirect genetic effects explain 36-40% of population polygenic score associations. However, indirect genetic effects are lower for achievement in the Dutch cohort, and for the adoption design. We identify causes of higher sibling- and trio-based estimates: prenatal indirect genetic effects, population stratification, and assortative mating. Our phenotype-agnostic, genetically sensitive approach has established overall environmental effects of parents skills, facilitating future mechanistic work.

genetics↗

Seasonal environments drive convergent evolution of a faster pace-of-life in tropical butterflies

Global change can trigger shifts in habitat stability and shape the evolution of organismal life-history strategies, with unstable habitats typically favouring a faster pace-of-life. We test this hypothesis in species-rich Mycalesina butterflies that have undergone parallel radiations in Africa, Asia, and Madagascar. First, our ancestral state reconstruction of habitat preference, using ~85% of extant species, revealed that early forest-linked lineages began to invade seasonal savannahs during the Late Miocene-Pliocene. Second, rearing replicate pairs of forest and savannah species from the African and Malagasy radiation in a common garden experiment, and utilising published data from the Asian radiation, demonstrated that savannah species consistently develop faster, have smaller bodies, higher fecundity with an earlier investment in reproduction, and reduced longevity, compared to forest species across all three radiations. We argue that time-constraints for reproduction favoured the evolution of a faster pace-of-life in savannah species that facilitated their persistence in seasonal habitats.

evolutionary biology↗

Multidimensional plasticity in the Glanville fritillary butterfly: larval performance curves are 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 environmentally induced variation, i.e. the consequences of potential maternal oviposition choices, in a suite of life-history traits in pre-diapause larvae of the Glanville fritillary butterfly. We focus on offspring survival, early growth rates and relative fat reserves, and pay specific attention to intraspecific variation in the responses (GxExE). Globally, we found that 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 other environmental variables. Interestingly, we find that 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. Altogether, the results of our study underscore the importance of paying attention to intraspecific trait variation in the field of evolutionary ecology.

evolutionary biology↗

A release from developmental bias accelerates morphological diversification in butterfly eyespots

Development can bias the independent evolution of traits sharing ontogenetic pathways, making certain evolutionary changes less likely. The eyespots commonly found on butterfly wings each have concentric rings of differing colors and these serially repeated pattern elements have been a focus for evo-devo research. In the butterfly family Nymphalidae, eyespots have been shown to function in startling or deflecting predators, and to be involved in sexual selection. Previous work on a model species of Mycalesina butterfly, Bicyclus anynana, has provided insights into the developmental control of the size and color composition of individual eyespots. Experimental evolution has also shown that the relative size of a pair of eyespots on the same wing surface is highly flexible, whereas they are resistant to diverging in color-composition, presumably due to the underlying shared developmental process. This fixed color-composition has been considered as a prime example of developmental bias with significant consequences for wing pattern evolution. Here we test this proposal by surveying eyespots across the whole subtribe of Mycalesina butterflies and demonstrate that developmental bias shapes evolutionary diversification, except in the genus Heteropsis which has gained independent control of eyespot color-composition. Experimental manipulations of pupal wings reveal that the bias has been released through a novel regional response of the wing tissue to a conserved patterning signal. Our study demonstrates that development can bias the evolutionary independence of traits, but it also shows how bias can be released through developmental innovations, thus allowing rapid morphological change, facilitating evolutionary diversification.

evolutionary biology↗

Investigating the Genetic Architecture of Non-Cognitive Skills Using GWAS-by-Subtraction

Educational attainment (EA) is influenced by cognitive abilities and by other characteristics and traits. However little is known about the genetic architecture of these "non-cognitive" contributions to EA. Here, we use Genomic Structural Equation Modelling and results of prior genome-wide association studies (GWASs) of EA (N = 1,131,881) and cognitive test performance (N = 257,841) to estimate SNP associations with variation in EA that is independent of cognitive ability. We identified 157 genome-wide significant loci and a polygenic architecture accounting for 57% of genetic variance in EA. Phenotypic and biological annotation revealed that (1) both cognitive and non-cognitive contributions to EA were genetically correlated with socioeconomic success and longevity; and (2) non-cognitive contributions to EA were related to personality, decision making, risk-behavior, and increased risk for psychiatric disorders; (3) non-cognitive and cognitive contributions to EA were enriched in the same tissues and cell types, but (4) showed different associations with gray-matter neuroimaging phenotypes.

genetics↗

Summer drought decreases the predictability of local extinctions in a butterfly metapopulation

The ecological impacts of extreme climatic events on population dynamics and/or community composition are profound and predominantly negative. Here, using extensive data of an ecological model system, we test whether predictions from ecological models remain robust when environmental conditions are outside the bounds of observation. First, we report a 10-fold demographic decline of the Glanville fritillary butterfly metapopulation on the [A]land islands (Finland). Next, using climatic and satellite data we show that the summer of 2018 was an anomaly in terms of water balance and vegetation productivity indices across the habitats of the butterfly, and demonstrate that population growth rates are strongly associated with spatio-temporal variation in climatic water balance. Finally, we demonstrate that covariates that have previously been identified to impact the extinction probability of local populations in this system are less informative when populations are exposed to (severe) drought during the summer months. Our results highlight the unpredictable responses of natural populations to extreme climatic events.

ecology↗

Intergenerational transmission of education and ADHD: Effects of parental genotypes

It is challenging to study whether children resemble their parents due to nature, nurture, or a mixture of both. Here we used a novel design that employs the fact that parents transmit 50% of their alleles to their offspring. The combined effect of these transmitted and non-transmitted alleles on a trait are summarized in a polygenic score (PGS). The non-transmitted PGS can only affect offspring through the environment, via genetically influenced behaviours in the parents, called genetic nurturing. For genotyped mother-father-offspring trios (1,120-2,518 per analysis) we calculated transmitted and non-transmitted PGSs for adult educational attainment (EA) and childhood ADHD and tested if these predicted outcomes in offspring. In adults, both transmitted (R2 = 7.6%) and non-transmitted (R2 = 1.7%) EA PGSs predicted offspring EA, evidencing genetic nurturing. In children around age 12, academic achievement was predicted only by transmitted EA PGSs (R2 = 5.7%), but we did not find genetic nurturing (R2 [~] 0.1%). The ADHD PGSs did not significantly predict academic achievement (R2 [~] 0.6%). ADHD symptoms in children were predicted by transmitted EA PGSs and ADHD PGSs (R2 = 1-2%). Based on these results, we conclude that previously reported associations between parent characteristics and offspring outcomes seem to be mainly a marker of genetic effects shared by parents and children.

genomics↗

Seasonal plasticity for anti-predatory strategies: matching colour and colour preference for effective crypsis

Effective anti-predatory strategies typically require matching appearance and behavior in prey, and there are many compelling examples of behavioral repertoires that enhance the effectiveness of morphological defenses. When protective adult morphology is induced by developmental environmental conditions predictive of future predation risk, adult behavior should be adjusted accordingly to maximize predator avoidance. While behavior is typically strongly affected by the adult environment, developmental plasticity in adult behavior -- mediated by the same pre-adult environmental cues that affect morphology -- could ensure an effective match between anti-predatory morphology and behavior. The coordination of environmentally-induced responses may be especially important in populations exposed to predictable environmental fluctuations (e.g. seasonality). Here, we studied early and late life environmental effects on a suite of traits expected to work together for effective crypsis. We focused on wing color and background color preference in Bicyclus anynana, a model of developmental plasticity that relies on crypsis as a seasonal strategy for predator avoidance. Using a full-factorial design, we disentangled effects of developmental and adult ambient temperature on both appearance and behavior. We showed that developmental conditions affect both adult color and color preference, with temperatures that simulate natural dry season conditions leading to browner butterflies with a perching preference for brown backgrounds. This effect was stronger in females, especially when butterflies were tested at lower ambient temperatures. In contrast to the expectation that motionlessness enhances crypsis, we found no support for our hypothesis that the browner dry-season butterflies would be less active. We argue that the integration of developmental plasticity for morphological and behavioral traits might improve the effectiveness of seasonal anti-predatory strategies. IMPACT SUMMARY To avoid predation, prey rely on strategies that typically include a variety of morphological and behavioral characteristics working together to deceive or scare predators. While some protective traits are a constitutive property of the prey species (e.g. hedgehog spines), others are produced only when the risk of encountering predators is high. For example, Daphnia crustaceans develop protective helmets and spines when exposed to cues that signal predator presence. When anti-predator morphologies are environmentally-induced, or plastic, the responses of associated behavioral traits should also be environmentally-dependent to ensure that animals exhibit behavioral repertoires that match their appearance. We used the tropical butterfly Bicyclus anynana, the squinting bush brown, to study these coordinated responses. In its natural habitat, with alternating dry and wet seasons, this thermally plastic butterfly alternates between seasonal forms with distinct wing color patterns related to distinct strategies to avoid predation. Dry season individuals, which develop under cooler temperatures, have small pattern elements on their wings and are cryptic against the brown background of dry foliage. In contrast, wet season individuals have large ornamental pattern elements that deflect attacks from predators towards the wing margin and away from their vulnerable bodies. We tested whether the cooler temperatures of the dry season also influenced other traits that can presumably improve the effectiveness of camouflage. In particular, we found that both the ornamental colors (appearance) and the choice of resting background colors (behavior) were affected by the temperature experienced during development. We found that dry season temperatures lead to browner butterflies with a stronger preference to rest on brown backgrounds. While behavior is typically very flexible in relation to changes in the adult environment, a developmental imprint on adult behavior can help ensure an effective match between the cryptic appearance and background choice behavior.

evolutionary biology↗

Complex effects of day and night temperature fluctuations on thermally plastic traits in an experimental model of adaptive seasonal plasticity.

BackgroundChanges in development in response to seasonally variable environments can produce phenotypes adjusted to fluctuating seasonal conditions and help organisms cope with temporal heterogeneity. In contrast to what happens in natural situations, experimental studies of developmental plasticity typically use environmental factors held constant during development, precluding assessment of potential environment-by-environment interaction effects.\n\nResultsWe tested effects of circadian fluctuations in temperature on a series of thermally plastic traits in a model of adaptive seasonal plasticity, the butterfly Bicyclus anynana. Comparing phenotypes from individuals reared under two types of fluctuations (warmer days with cooler nights, and cooler days with warmer nights) and those reared under a constant temperature of the same daily average allowed us to identify complex patterns of response to day and night temperatures. We found evidence of additive-like effects (for body size), but also different types of \"dominance\"-type effects where one particular period of the light cycle (for development time) or one particular extreme temperature (for eyespot size) had a relatively larger contribution to phenotype expression. We also gathered evidence against the hypothesis that thermal plasticity in development time drives thermal plasticity in other traits.\n\nConclusionsCombined effects of fluctuating day and night temperatures include additive-like effects as well as different types of environmental-dominance interaction effects. Differences between plastic traits reveal independent responses to temperature, and possible independent assessment of temperature conditions. Our study underscores the importance of understanding how organisms integrate complex environmental information towards a complete understanding of natural phenotypic variation and of the potential impact of environmental change thereon.

evolutionary biology↗