Article

Testing the migration syndrome: Comparative fecundity of migratory and non‐migratory nymphaline butterflies

Authors:
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

Empirical studies have shown a positive relationship between migration and fecundity, suggesting a ‘migration syndrome’ that also includes delayed reproduction and an extended reproductive lifespan. At the same time, life history theory predicts that the cost of migration should result in lower fecundity because both traits draw from a common resource. We test whether migration is associated with higher fecundity and delayed reproduction in five closely related butterfly species in the Nymphalini tribe. Two of these are migratory, Vanessa cardui and Vanessa atalanta , and three are non‐migratory, Aglais urticae , Aglais io , and Polygonia c‐album , which appears in a diapausing and a non‐diapausing generation. Laboratory experiment of this study demonstrated a higher lifetime fecundity in the non‐migratory species A. urticae and A. io , compared with the migratory species. When reproductive output was measured in terms of egg mass over adult female mass, also the non‐migratory species P. c‐album had a higher reproductive investment than the two migratory species, and the non‐diapausing generation had a higher reproductive output than the diapausing generation. All species but P. c‐album delayed reproduction until 5–7 days after eclosion/emergence. These results indicate that a migratory lifestyle carries a reproductive cost and suggests that the migratory habit has not resulted in selection for higher fecundity. However, the migratory species are highly fecund in a wider phylogenetic perspective, which leads to the conclusion that rather than selection having selected for high fecundity and delayed reproduction, these traits may be prerequisites for evolving a migratory lifestyle.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... Insects need to balance energy allocation between migration and reproduction (Minter et al., 2018). Many insects exhibit the "oogenesis-flight" syndrome, where egg development and mating are suppressed during migration and only commence after it, whereas nonmigratory individuals can quickly reach sexual maturity and allocate resources to reproduction immediately after eclosion (Jiang et al., 2011;Minter et al., 2018;Wiklund & Friberg, 2022). Compared to migratory butterflies, their closely related non-migratory congeners begin reproduction more quickly after eclosion (Wiklund & Friberg, 2022). ...
... Many insects exhibit the "oogenesis-flight" syndrome, where egg development and mating are suppressed during migration and only commence after it, whereas nonmigratory individuals can quickly reach sexual maturity and allocate resources to reproduction immediately after eclosion (Jiang et al., 2011;Minter et al., 2018;Wiklund & Friberg, 2022). Compared to migratory butterflies, their closely related non-migratory congeners begin reproduction more quickly after eclosion (Wiklund & Friberg, 2022). Therefore, the migratory individuals of the Ghanaian FAW may have a later sexual maturity period compared to non-migratory individuals. ...
Article
Full-text available
The fall armyworm (FAW), an important migratory pest native to the Amer-icas, was first detected in a nonnative region (West Africa) in 2016. In the following years, it quickly spread to multiple regions worldwide. FAW exhibits long-distance seasonal migration in both the Americas and Asia, primarily to take advantage of suitable seasonal habitats as they appear along the migratory pathways. Tropical West Africa experiences minimal annual temperature variation and has widely distributed potential year-round habitats, leading us to hypothesize that the migration capacity of FAW populations in this region may be substantially reduced. To test our hypothesis, we assessed the flight performance of FAW collected from Ghana in West Africa with tethered flight mills and compared it to that of a FAW population from southern China. Additionally, we quantified the relationships between morphological characteristics and flight performance of the FAW from Ghana. Based on observed flight behaviors, we categorized FAW into migratory and non-migratory types. The flight capabilities of first-generation Ghanaian FAW bred in the laboratory were similar to that of the field population from Yunnan, Southwest China, with migrants making up the majority. However, after several generations of laboratory rearing, the flight capability of the Ghanaian population significantly declined, primarily due to a marked increase in the proportion of non-migratory individuals. The low correlation between morphological variables and flight duration suggests that genetic factors likely determine most variations in flight propensity. The results of this study indicate that FAW with high migratory capacity in West Africa is likely to pose a threat to crops in eradication zones and neighboring uninvaded areas and may possibly be capable of crossing the Sahara Desert and invading Europe. Therefore, it is crucial to establish comprehensive pest early warning and management systems.
... The painted lady (Vanessa cardui) is an emerging model system for investigating migratory behaviour in insects (García-Berro et al., 2023;Menchetti et al., 2019;Näsvall et al., 2023;Shipilina et al., 2022;Stefanescu et al., 2013Stefanescu et al., , 2017Stefanescu et al., , 2021Suchan et al., 2019;Talavera et al., 2018;Wiklund & Friberg, 2022). Besides being the most widespread of all butterflies-the species distribution is almost worldwide-the painted lady is also the butterfly migrating the longest distances (Talavera et al., 2018;Talavera & Vila, 2017). ...
Article
Seasonal environmental fluctuations provide formidable challenges for living organisms, especially small ectotherms such as butterflies. A common strategy to cope with harsh environments is to enter diapause, but some species avoid unsuitable conditions by migrating. Despite a growing understanding of migration in the life cycles of some butterfly species, it remains unknown how individuals register and store environmental cues to determine whether and where to migrate. Here, we explored how competition and host plant availability during larval development affect patterns of DNA methylation in the migratory painted lady (Vanessa cardui) butterfly. We identify a set of potentially functional methylome shifts associated with differences in the environment, indicating that DNA methylation is involved in the response to different conditions during larval development. By analysing the transcriptome for the same samples used for methylation profiling, we also uncovered a non-monotonic relationship between gene body methylation and gene expression. Our results provide a starting point for understanding the interplay between DNA methylation and gene expression in butterflies in general and how differences in environmental conditions during development can trigger unique epigenetic marks that might be important for behavioural decisions in the adult stage.
... Cecil G. Johnson studied differences in life history traits between migratory and nonmigratory butterflies, showing that (i) migratory females start their flight before ovarian development, (ii) migrants are sexually immature in some cases, (iii) migratory individuals usually gain weight as they fuel up for the long journey, and (iv) they have longer forewings than nonmigrant individuals (Johnson, 1963(Johnson, , 1966(Johnson, , 1969Stefanescu et al., 2021;Wiklund & Friberg, 2022). This work suggested that distinctive physiological and neurophysiological factors are associated with migration, and that ovarian development can be initiated, prolonged, or suppressed depending on the environmental conditions. ...
Article
Full-text available
Several hundred butterfly species show some form of migratory behaviour. Here we identify how the methodologies available for studying butterfly migration have changed over time, and document geographic and taxonomic foci in the study of butterfly migration. We review publications on butterfly migration published in six languages (English, Simplified Chinese, Traditional Chinese, Japanese, Korean, and Spanish), summarise how migration in butterflies has been studied, explore geographic and taxonomic patterns in the knowledge base, and outline key future research directions. Using English search keywords, we found only 58 studies from Asia; however, after searching in local languages, we found an additional 98 relevant studies. Overall, butterfly migration studies are mostly from North America and Europe. Most studies focus on three species: monarch (Danaus plexippus), painted lady (Vanessa cardui) and red admiral (Vanessa atalanta). About 62% of publications are focused on the monarch, with nearly 50% of migratory butterfly species mentioned in only a single paper. Several research methods have been applied to ascribe migratory status and to study the physiology, neurobiology, and ecology of migration; however, virtually all this research is on a handful of species. There remain hundreds of species for which we do not understand the comprehensive seasonal pattern of movement, flight destinations, wintering, or breeding grounds. A better understanding of movement ecology and migratory connectivity is needed to effectively conserve migratory butterflies. It is essential that research becomes more geographically and linguistically representative since migrants frequently cross political borders and international cooperation is necessary for their conservation.
... As a typical r-strategist migratory insect, large population sizes may be advantageous in exploiting ephemeral flush vegetation, as well as in balancing the cost of higher mortality rates associated with migration (Dingle, 1978;Hill, 1983;Chapman et al., 2015). Moreover, the species has high reproductive potential (varying over several orders of magnitude in comparison to vertebrates), where single females may lay >1000 eggs (Benyamini, 2017;Wiklund & Friberg, 2022), and can eventually behave as pests in particular breeding sites. Lastly, migration also facilitates higher population sizes by allowing escape from high parasitoid loads, an important factor exerting population control in insects (Chapman et al., 2015;Jeffries & Lawton, 1984;Owen, 1987;Stefanescu et al., 2012). ...
Article
Full-text available
Migration is typically associated with risk and uncertainty at the population level, but little is known about its cost and benefit trade-offs at the species level. Migratory insects in particular often exhibit strong demographic fluctuations due to local bottlenecks and outbreaks. Here, we use genomic data to investigate levels of heterozygosity and long-term population size dynamics in migratory insects, as an alternative to classical local and short-term approaches such as regional field monitoring. We analyze whole-genome sequences from 97 Lepidoptera species and show that individuals of migratory species have significantly higher levels of genome-wide heterozygosity, a proxy for effective population size, than non-migratory species. Also, we contribute whole-genome data for one of the most emblematic insect migratory species, the painted lady butterfly (Vanessa cardui), sampled across its worldwide distributional range. This species exhibits one of the highest levels of genomic heterozygosity described in Lepidoptera (2.95% ± 0.15). Coalescent modeling (PSMC) shows historical demographic stability in V. cardui, and high effective population size estimates of 2 to 20 million individuals 10,000 years ago. The study reveals that the high risks associated with migration and local environmental fluctuations do not seem to decrease overall genetic diversity and demographic stability in migratory Lepidoptera. We propose a "compensatory" demographic model for migratory r-strategist organisms in which local bottlenecks are counterbalanced by reproductive success elsewhere within their typically large distributional ranges. Our findings highlight that the boundaries of populations are substantially different for sedentary and migratory insects, and that, in the latter, local and even regional field monitoring results may not reflect whole population dynamics. Genomic diversity patterns may elucidate key aspects of an insect's migratory nature and population dynamics at large spatiotemporal scales.
Article
Full-text available
The painted lady butterfly Vanessa cardui is renowned for its virtually cosmopolitan distribution and the remarkable long-distance migrations as part of its annual, multigenerational migratory cycle. In winter, V. cardui individuals inhabit breeding grounds north and south of the Sahara, suggesting distinct migratory behaviors within the species as individuals migrate southward from Europe in the autumn. However, the evolutionary and ecological factors shaping these differences in migratory behavior remain largely unexplored. Here, we performed whole-genome resequencing and analyzed the hydrogen and strontium isotopes of 40 V. cardui individuals simultaneously collected in the autumn from regions both north and south of the Sahara. Our investigation revealed two main migratory groups: (i) short-distance migrants, journeying from temperate Europe to the circum-Mediterranean region and (ii) long-distance migrants, originating from Europe, crossing the Mediterranean Sea and Sahara, and reaching West Africa, covering up to over 4,000 km. Despite these stark differences in migration distance, a genome-wide analysis revealed that short- and long-distance migrants belong to a single intercontinental panmictic population extending from northern Europe to sub-Saharan Africa. Contrary to common biogeographic patterns, the Sahara is not a catalyst for population structuring in this species. No significant genetic differentiation or signs of adaptation and selection were observed between the two migratory phenotypes. Nonetheless, two individuals, who were early arrivals to West Africa covering longer migration distances, exhibited some genetic differentiation. The lack of genetic structure between short- and long-distance migrants suggests that migration distance in V. cardui is a plastic response to environmental conditions.
Chapter
Entomologists recognize migratory behavior as persistent and straightened-out locomotory activity that enables pre-emptive escape from ephemeral habitats before they deteriorate and timely colonization of newly favorable ones. It manifests as (i) directed low-altitude movement by day, generally using sun compass orientation; (ii) daytime ascent to altitude utilizing lift from turbulent convection followed by downwind drift; or (iii) active ascent at dusk followed by oriented but predominantly windborne movement at altitudes with favorable temperatures and windspeeds. Many migratory insect species are agricultural pests or vectors of human, animal, or plant diseases; others have beneficial economic and societal impacts.
Preprint
The painted lady butterfly Vanessa cardui is renowned for its virtually cosmopolitan distribution and the remarkable long-distance migrations that are part of its annual, multi-generational migratory cycle. Recently, V. cardui individuals were found north and south of the Sahara in the autumn, suggesting distinct migratory behaviours within the species. However, the evolutionary and ecological factors shaping these differences in migratory behaviour remain largely unexplored. Here, we performed whole-genome resequencing and analysed the hydrogen and strontium isotopes of 40 V. cardui individuals simultaneously collected in the autumn from regions both north and south of the Sahara. Our investigation revealed two main migratory groups: (i) short-distance migrants, journeying from temperate Europe to the circum-Mediterranean region and (ii) long-distance migrants, originating from Europe, crossing the Mediterranean Sea and Sahara, and reaching West Africa, covering up to over 4,000 km. Despite these stark differences in migration distance, a genome-wide analysis revealed that both short- and long-distance migrants belong to a single intercontinental panmictic population extending from northern Europe to sub-Saharan Africa. Contrary to common biogeographic patterns, the Sahara is not a catalyst for population structuring in this species. No significant genetic differentiation or signs of adaptation and selection were observed between the two migratory phenotypes (pairwise F ST = 0.001 ± 0.006). Nonetheless, two individuals, which were early arrivals to West Africa and covered longer migration distances, exhibited some genetic differentiation. The lack of genetic structure between short- and long-distance migrants suggests that migration distance in V. cardui is a plastic response to environmental conditions. Significance statement Although migratory insects dominate living biomass fluxes and impact agriculture, ecosystems, and human communities, little is known about the controls of their migratory behavior. Our study develops an interdisciplinary framework, applied to the migratory butterfly V.cardui , to explore the genetic basis of variation in insect migration behavior. We leverage new generation isotope geolocation techniques to uncover striking differences in butterfly behaviour, with some individuals migrating short distances within the circum-Mediterranean region and others migrating thousands of kilometers across the Mediterranean Sea and Sahara. This major difference does not coincide with genetic differentiation or population structure and is likely a plastic response to environmental cues. This study provides a ground-breaking framework to study migration in insects.
Article
Full-text available
Significance The painted lady butterfly is an annual migrant to northern regions, but the size of the immigration varies by more than 100-fold in successive years. Unlike the monarch, the painted lady breeds year round, and it has long been suspected that plant-growing conditions in winter-breeding locations drive this high annual variability. However, the regions where caterpillars develop over winter remained unclear. Here, we show for the European summer population that winter plant greenness in the savanna of sub-Saharan Africa is the key driver of the size of the spring immigration. Our results show that painted ladies regularly cross the Sahara Desert and elucidate the climatic drivers of the annual population dynamics.
Article
Full-text available
Insect populations including butterflies are declining worldwide, and they are becoming an urgent conservation priority in many regions. Understanding which butterfly species migrate is critical to planning for their conservation, because management actions for migrants need to be coordinated across time and space. Yet, while migration appears to be widespread among butterflies, its prevalence, as well as its taxonomic and geographic distribution are poorly understood. The study of insect migration is hampered by their small size and the difficulty of tracking individuals over long distances. Here we review the literature on migration in butterflies, one of the best‐known insect groups. We find that nearly 600 butterfly species show evidence of migratory movements. Indeed, the rate of ‘discovery’ of migratory movements in butterflies suggests that many more species might in fact be migratory. Butterfly migration occurs across all families, in tropical as well as temperate taxa; Nymphalidae has more migratory species than any other family (275 species), and Pieridae has the highest proportion of migrants (13%; 133 species). Some 13 lines of evidence have been used to ascribe migration status in the literature, but only a single line of evidence is available for 92% of the migratory species identified, with four or more lines of evidence available for only 10 species – all from the Pieridae and Nymphalidae. Migratory butterflies occur worldwide, although the geographic distribution of migration in butterflies is poorly resolved, with most data so far coming from Europe, USA, and Australia. Migration is much more widespread in butterflies than previously realised – extending far beyond the well‐known examples of the monarch Danaus plexippus and the painted lady Vanessa cardui – and actions to conserve butterflies and insects in general must account for the spatial dependencies introduced by migratory movements.
Article
Full-text available
Insects in temperate areas spend the inhospitable winter conditions in a resting stage known as diapause. In species that diapause in the larval or pupal stage, the decision whether to diapause or develop directly is customarily taken during the late instars, with long days (i.e., long light phases) and high temperatures promoting direct development. Among butterflies that overwinter as adults, data are rare and variable, but imply that the larval daylength conditions can affect the pathway decision. We studied the small tortoiseshell, Aglais urticae L. (Lepidoptera: Nymphalidae, Nymphalini), which is partially bivoltine from Central Scandinavia and southwards, and tested whether the pathway decision is taken in the larval or adult stage. We reared larvae under long‐day (L22:D2) or short‐day (L12:D12) photoperiods, and recorded the pathway taken by the eclosing adults by scoring their propensity to mate and produce eggs. We also tested whether the larval photoperiod influenced adult ability to diapause by assessing adult survival. The results clearly indicate that (1) there is no detectable effect of larval photoperiod treatment on the pathway decision taken by adults whether to enter diapause or to develop directly, (2) some individuals are obligately univoltine and insensitive to photoperiod during adulthood, whereas (3) other individuals can facultatively enter diapause or direct development, depending on the photoperiod experienced after adult eclosion. Insects with two or more generations per year typically decide whether to overwinter or develop directly without diapause, using daylight and temperature as cues. This decision is almost always made during the larval stages – also in species that overwinter as adults. We demonstrate that in Aglais urticae (Lepidoptera: Nymphalidae), the pathway decision is made in the adult stage. This is the first demonstration of the pathway decision being made in the adult stage in a butterfly that overwinters as adult.
Article
Full-text available
Migratory behaviour has repeatedly evolved across taxa as an adaptation to heterogeneity in space and time. However, insect migration is still poorly understood, partly because of the lack of field data. The painted lady butterfly Vanessa cardui undertakes a long-distance annual migration between Europe and Africa. While spring flights from the Maghreb to Europe are well characterized, it is not known how far the European autumn migrants travel into Africa and whether they massively cross the Sahara Desert. We conducted fieldwork in four African countries (Chad, Benin, Senegal, and Ethiopia) in autumn and documented southward migrants in central Chad and abundant breeding sites across the tropical savannah as far south as the Niger River in the west and the Ethiopian highlands in the east. Given directionality and timing, these migrants probably originated in Europe and crossed the Mediterranean, the Sahara and the Sahel, a hypothesis that implies the longest (>4000 km) migratory flight recorded for a butterfly in a single generation. In the light of the new evidence, we revise the prevailing spatiotemporal model for the annual migration of V. cardui to incorporate tropical Africa, which could potentially be regarded as the missing geographic link between autumn (southwards) and spring (northwards) movements.
Article
Full-text available
Most butterfly species can be characterized as capital breeders, meaning that reproductive output is strongly coupled to the amount of resources they have procured during the larval stage. Accordingly, female fecundity is generally correlated with female mass, both within and across species. However, the females of some species can be partly characterized as income breeders. in the sense that their reproductive output is dependent not only on larval-derived capital but also on resources acquired during the adult stage. These adult resources can be derived from female feeding or from male-transferred nuptial gifts. Recent studies on the within-species effects of multiple matings on female fitness show that females generally gain directly from multiple matings in terms of increased lifetime offspring production. Here, we test whether the positive effects of multiple mating on female fitness also hold at a comparative level, by conducting a laboratory study of female reproductive output in eight pierid species that differ in lifetime female mating frequency. Female reproductive output, measured as cumulative egg mass divided by female mass, increased significantly with polyandry (r = 0.942, p < 0.001), demonstrating that the positive effect of mating rate on female reproductive fitness also holds between species. The positive effect of male nutrient contribution is substantial, and the per capita reproductive output is more than twice as high in the most polyandrous species as in the most monandrous ones. Hence, the positive net effect of the ejaculates is highly substantial, although males and females can have sexual interests that run counter to each other, setting the stage for sexually antagonistic coevolution, so that the various component parts of the male ejaculate-sperm, nutrients, anti-aphrodisiacs, and gonadotrophic hormones-may each correspond to a separate conflict-cooperation balance between the sexes. Two scenarios for the evolution of nuptial gifts in butterflies are discussed, one arguing that variation in larval food is the underlying factor and the other arguing that sexually antagonistic coevolution is the driving force. The two views are complementary rather than mutually exclusive, although the former hypothesis predicts that variation in female mating rate depends on variation in larval food availability, whereas the latter suggests that variation in female mating rate between species results from species-specific idiosyncrasies.
Article
Full-text available
Dispersal, the behaviour ensuring gene flow, tends to covary with a number of morphological, ecological and behavioural traits. While species-specific dispersal behaviours are the product of each species' unique evolutionary history, there may be distinct interspecific patterns of covariation between dispersal and other traits ('dispersal syndromes') due to their shared evolutionary history or shared environments. Using dispersal, phylogeny and trait data for 15 terrestrial and semi-terrestrial animal Orders (> 700 species), we tested for the existence and consistency of dispersal syndromes across species. At this taxonomic scale, dispersal increased linearly with body size in omnivores, but decreased above a critical length in herbivores and carnivores. Species life history and ecology significantly influenced patterns of covariation, with higher phylogenetic signal of dispersal in aerial dispersers compared with ground dwellers and stronger evidence for dispersal syndromes in aerial dispersers and ectotherms, compared with ground dwellers and endotherms. Our results highlight the complex role of dispersal in the evolution of species life-history strategies: good dispersal ability was consistently associated with high fecundity and survival, and in aerial dispersers it was associated with early maturation. We discuss the consequences of these findings for species evolution and range shifts in response to future climate change.
Article
Full-text available
We have used a comparative approach in order to understand what determines egg size by analyzing relationships of egg to female body size in 11 pierid and 17 satyrid butterflies. Adult female weight varies between 30 mg and 300 mg, and since scaling of morphological character traits is usually observed, we would expect a positive correlation between egg and female size as a result of nonadaptive allometry (in the sense of Huxley 1932) in the absence of selective pressures on egg size. However, two such pressures can readily be recognized, both of which should cause egg size to depart from the baseline allometry. First, a positive correlation between egg size and offspring fitness may select for bigger eggs. Second, since there is a negative relationship between egg size and fecundity, selection on females to maximize fecundity confers a selective pressure to decrease egg size. Since these selective pressures signify a parent-offspring conflict, we follow Parker and Begon's assumption that "selection acts ...
Article
Full-text available
Females of three tropical satyrine butterflies in the genus Mycalesis lay variable-sized eggs. The species also differ substantially in their mean egg weights with M. perseus laying smaller eggs than M. terminus and M. sirius. The adaptive significance of the egg size variation was examined in relation to three offspring fitness components: larval survival, larval developmental time and pupal weight, to establish if larvae derived from heavier eggs were in any way better than those derived from lighter eggs when reared on different hostplant qualities varying in leaf toughness and nitrogen content. When the three species were reared on the tougher nitrogen-poor host quality (Panicum-intermediate category) larvae from heavier eggs had significantly better chance of surviving and reaching adulthood than those from lighter eggs. However, when larvae were reared on the softer nitrogen-rich host quality (Panicum-soft category) the advantage to heavier eggs diminished in M. terminus and M. sirius, but not in M. perseus. Egg weight was also positively correlated with subsequent pupal weight in M. perseus for both male and female larvae reared on Panicum-soft, and with larval development rate in M. sirius (both sexes) when reared on Themeda - a hostplant known to be of poor quality for M. sirius. The positive correlation between egg size and offspring fitness suggests that under field conditions larvae from larger eggs may do better than those from smaller eggs when conditions are unfavourable, for example, adverse climate or poor host quality. Moreover, a strong positive correlation between egg size and the width of the head capsule of newly emerged first instar larvae suggests that larvae from larger eggs have bigger mandibles and therefore potentially able to chew and survive better on tougher foliage. Potential selective pressures likely to influence egg size in these satyrines and other butterflies are discussed.
Article
Full-text available
For animals in general, a benefit of group living may be a decreased risk of predator attack on any particular individual. For insects, this dilution effect can be a consequence of distastefulness, which limits the number of prey that a predator can take. A model is developed in which risk of detection is varied in relation to group size and degree of prey distastefulness and aposematic coloration, both of which affect the number of prey a predator samples during avoidance learning. Members of small groups may have a higher rate of death from predation than solitary individuals, but above a certain minimum group size, group members do better than solitary individuals. Factors unrelated to predation constrain group size. Such constraints must be weak enough to allow groups larger than the minimum size. The model predicts that 1) gregarious insect species should be distasteful, and evolution of distastefulness should precede that of gregariousness; 2) distribution of group sizes among species should show a bimodal form; and 3) largest aggregations should be found in forms that have fewer constraints unrelated to predation on group size. -from Authors
Article
Full-text available
Little is known of the population dynamics of long-range insect migrants, and it has been suggested that the annual journeys of billions of nonhardy insects to exploit temperate zones during summer represent a sink from which future generations seldom return (the "Pied Piper" effect). We combine data from entomological radars and ground-based light traps to show that annual migrations are highly adaptive in the noctuid moth Autographa gamma (silver Y), a major agricultural pest. We estimate that 10-240 million immigrants reach the United Kingdom each spring, but that summer breeding results in a fourfold increase in the abundance of the subsequent generation of adults, all of which emigrate southward in the fall. Trajectory simulations show that 80% of emigrants will reach regions suitable for winter breeding in the Mediterranean Basin, for which our population dynamics model predicts a winter carrying capacity only 20% of that of northern Europe during the summer. We conclude not only that poleward insect migrations in spring result in major population increases, but also that the persistence of such species is dependent on summer breeding in high-latitude regions, which requires a fundamental change in our understanding of insect migration.
Article
Full-text available
Summary • Evolutionary theory predicts that resource allocation decisions taken during development are adjusted to an organism's life-history. These decisions may have irreversible effects on body design and strong fitness consequences. Holometabolous insects that have a long expected life span typically postpone reproduction, and so are expected to allocate resources for somatic maintenance prior to investing in reproduction. In contrast, insects that have a short expected life span are expected to allocate relatively less to soma and more to reproduction. In support of this theory, an earlier investigation of resources allocated to soma vs. reproductive reserves in the comma butterfly, Polygonia c-album, revealed that short-lived females indeed allocate more resources to reproductive reserves as compared to longer lived females that hibernate before reproduction suggesting that short-lived females should have higher fecundity. • Here we test this prediction, using the comma butterfly as our study organism. Depending on daylength and temperature this butterfly produces one of two morphs: (i) a light summer morph that reproduces directly after adult eclosion and has a short expected life span of a couple of weeks; or (ii) a darker winter morph that normally lives for 8–9 months before the onset of reproduction. Our test is based on experimental manipulation that allowed us to induce reproduction without prior hibernation in winter morph comma butterflies, and comparing lifetime fecundity among three groups: (i) directly reproducing summer morph commas; (ii) directly reproducing winter morph commas; and (iii) winter morph commas reproducing after overwintering. This protocol allowed us to tease apart trade-offs during development and the hibernation period. • The results showed that the short-lived summer morph had a substantially higher fecundity (total number of eggs = 586 ± 19, mean ± SE) than the winter morph females manipulated to reproduce without hibernation (total number of eggs = 334 ± 42). We argue that this is a consequence of a resource allocation trade-off during early development observed in this species; females with a short expected life as adults allocate relatively more of their resources to reproductive parts and thereby reach a higher reproductive output compared to females predisposed for a long adult life. • There was no significant difference in lifetime fecundity between winter morph females that did, or did not, hibernate before reproduction. This suggests that the cost of hibernation per se is small and hence corroborates our conclusion that the life-history implemented trade-off made during early development underlies the lower reproductive output of the winter morph butterflies.
Article
Full-text available
1. Many studies have identified different factors influencing clutch‐size regulation, primarily within various groups of insects. One prediction is that ovipositing females should increase clutch size with host quality. However, in many studies it is not clear whether ovipositing females are responding to host quality or quantity. 2. Females of the polyphagous comma butterfly, Polygonia c‐album (L.), were allowed to oviposit on two hosts differing greatly in quality: the preferred host, stinging nettle ( Urtica dioica L.), and the low‐ranked host, birch ( Betula pubescens Ehrh). Ovipositing females were observed visually and clutch sizes were recorded. The experiment was repeated in three different years; in total, 938 observations of oviposition events were made. 3. In all three years, females ovipositing on U. dioica laid larger clutches (median 1.6–1.85) compared with females ovipositing on B. pubescens (median 1.0–1.3) . The difference was significant in two out of three years and when all three years were pooled. 4. Thus, P. c‐album females exhibit clutch‐size regulation, with larger clutches on better hosts. It is suggested that the proximate mechanism is likely to be a response to the same stimuli used for female ranking of host plants in the preference hierarchy.
Article
Full-text available
Insect size tactics or developmental strategies are discussed in relation to decisions individuals make about when to mature. Such decisions carry with them costs and benefits in terms of that individual's reproductive success. Whenever size affects fitness, selection should act such that individuals evaluate the costs and benefits due to changes in size and should mature when the ratio of benefit to cost is maximized. Predictions about seasonal changes in adult sizes within a population are tested on two species of mole cricket, Scapteriscus acletus and vicinus. Specifically, individuals maturing in the fall should be larger than average because there is no cost associated with delayed reproduction since reproduction occurs only during spring months. Smaller than average individuals should remain in juvenile stages and get larger before reproducing. Also it is predicted that as the spring reproductive season progresses a greater proportion of smaller individuals should mature because the costs due to delaying reproduction increase. The changes in seasonal distribution of adult sizes of mole crickets support the predictions and suggest that individuals make decisions about when to mature based on costs and benefits associated with changes in size.
Article
Full-text available
Insects that hibernate as adults have a life span of almost a whole year. Hence, they must have extraordinary adaptations for adult survival. In this paper, we study winter survival in two butterflies that hibernate as adults and have multimodal anti-predator defences—the peacock, Inachis io, which has intimidating eyespots that are effective against bird predation, and the small tortoiseshell, Aglais urticae, which does not have an effective secondary defence against birds. We assessed predation on wild butterflies hibernating in the attic of an unheated house, as well as survival of individually marked butterflies placed by hand on different sites in the attic. Our objectives were to assess (1) the number of butterflies that were killed during hibernation, (2) whether survival differed between butterfly species, and (3) how predation was related to hibernation site and the identity of the predator. There was a strong pulse of predation during the first 2weeks of hibernation: 58% of A. urticae and 53% of I. io were killed during this period. Thereafter, predation decreased and butterfly survival equalled 98% during the final 16weeks of hibernation. There was no difference in survival between the two butterfly species, but predation was site-specific and more pronounced under light conditions in locations accessible to a climbing rodent, such as the common yellow-necked mouse, Apodemus flavicollis. We contend that small rodents are likely important predators on overwintering butterflies, both because rodents are active throughout winter when butterflies are torpid and because they occur at similar sites.
Article
Full-text available
Vast numbers of insects and passerines achieve long-distance migrations between summer and winter locations by undertaking high-altitude nocturnal flights. Insects such as noctuid moths fly relatively slowly in relation to the surrounding air, with airspeeds approximately one-third of that of passerines. Thus, it has been widely assumed that windborne insect migrants will have comparatively little control over their migration speed and direction compared with migrant birds. We used radar to carry out the first comparative analyses of the flight behaviour and migratory strategies of insects and birds under nearly equivalent natural conditions. Contrary to expectations, noctuid moths attained almost identical ground speeds and travel directions compared with passerines, despite their very different flight powers and sensory capacities. Moths achieved fast travel speeds in seasonally appropriate migration directions by exploiting favourably directed winds and selecting flight altitudes that coincided with the fastest air streams. By contrast, passerines were less selective of wind conditions, relying on self-powered flight in their seasonally preferred direction, often with little or no tailwind assistance. Our results demonstrate that noctuid moths and passerines show contrasting risk-prone and risk-averse migratory strategies in relation to wind. Comparative studies of the flight behaviours of distantly related taxa are critically important for understanding the evolution of animal migration strategies.
Article
Full-text available
The "oscillation hypothesis" has been proposed as a general explanation for the exceptional diversification of herbivorous insect species. The hypothesis states that speciation rates are elevated through repeated correlated changes--oscillations--in degree of host plant specificity and geographic range. The aim of this study is to test one of the predictions from the oscillation hypothesis: a positive correlation between diet breadth (number of host plants used) and geographic range size, using the globally distributed butterfly subfamily Nymphalinae. Data on diet breadth and global geographic range were collected for 182 Nymphalinae butterflies species and the size of the geographic range was measured using a GIS. We tested both diet breadth and geographic range size for phylogenetic signal to see if species are independent of each other with respect to these characters. As this test gave inconclusive results, data was analysed both using cross-species comparisons and taking phylogeny into account using generalised estimating equations as applied in the APE package in R. Irrespective of which method was used, we found a significant positive correlation between diet breadth and geographic range size. These results are consistent for two different measures of diet breadth and removal of outliers. We conclude that the global range sizes of Nymphalinae butterflies are correlated to diet breadth. That is, butterflies that feed on a large number of host plants tend to have larger geographic ranges than do butterflies that feed on fewer plants. These results lend support for an important step in the oscillation hypothesis of plant-driven diversification, in that it can provide the necessary fuel for future population fragmentation and speciation.
Article
Full-text available
Many organisms delay the initiation of reproduction even though such delay is not adaptive in a constant environment. Theoretical arguments in this paper show that delaying reproduction can increase fitness in a sufficiently variable environment. This paper uses stochastic demography to analyze the fluctuating population structure produced by environmental uncertainty. The results explain previously puzzling features of life cycle delays observed in nature, predicting that populations of the same species living in environments of differing harshness can display different life history phenotypes, a number of distinct life history phenotypes can coexist neutrally within a single population, and genetic polymorphisms are easily maintained if heterozygotes have intermediate life history phenotypes.
Article
Full-text available
Most butterfly species can be characterized as capital breeders, meaning that reproductive output is strongly coupled to the amount of resources they have procured during the larval stage. Accordingly, female fecundity is generally correlated with female mass, both within and across species. However, the females of some species can be partly characterized as income breeders, in the sense that their reproductive output is dependent not only on larval-derived capital but also on resources acquired during the adult stage. These adult resources can be derived from female feeding or from male-transferred nuptial gifts. Recent studies on the within-species effects of multiple matings on female fitness show that females generally gain directly from multiple matings in terms of increased lifetime offspring production. Here, we test whether the positive effects of multiple mating on female fitness also hold at a comparative level, by conducting a laboratory study of female reproductive output in eight pierid species that differ in life-time female mating frequency. Female reproductive output, measured as cumulative egg mass divided by female mass, increased significantly with polyandry (r = 0.942, p < 0.001), demonstrating that the positive effect of mating rate on female reproductive fitness also holds between species. The positive effect of male nutrient contribution is substantial, and the per capita reproductive output is more than twice as high in the most polyandrous species as in the most monandrous ones. Hence, the positive net effect of the ejaculates is highly substantial, although males and females can have sexual interests that run counter to each other, setting the stage for sexually antagonistic coevolution, so that the various component parts of the male ejaculate-sperm, nutrients, anti-aphrodisiacs, and gonadotrophic hormones-may each correspond to a separate conflict-cooperation balance between the sexes. Two scenarios for the evolution of nuptial gifts in butterflies are discussed, one arguing that variation in larval food is the underlying factor and the other arguing that sexually antagonistic coevolution is the driving force. The two views are complementary rather than mutually exclusive, although the former hypothesis predicts that variation in female mating rate depends on variation in larval food availability, whereas the latter suggests that variation in female mating rate between species results from species-specific idiosyncrasies.
Article
In many migratory insects, migration occurs during the prereproductive phase of the life cycle. This trait probably arises from a trade-off between migration and reproduction and in females has been termed the ‘oogenesis–flight syndrome’. However, the generality of this syndrome has been questioned, especially for monomorphic insects. We studied the relationship between migration and reproduction in the highly cosmopolitan painted lady butterfly, Vanessa cardui, which in the Palaearctic undertakes the longest known multigenerational migration circuit of any insect. We tested for the oogenesis–flight syndrome in both spring and autumn migrants in two regions linked by migration, North Africa and northern Spain. Field observations were combined with laboratory experiments to determine the life span and the age at first mating to unravel the reproductive strategy observed in wild-caught individuals. Females and males wait on average around 5–6 days before mating, and field data revealed that mating frequencies increased rapidly once females reached a medium wing wear category. There were seasonal differences in mating frequencies in the study regions depending on whether the region acted as a source or as a destination for migrants, and in the latter case there were almost twice as many mated females. Moreover, a great majority of females collected during migratory flights were unmated, the remaining females having mated only very recently. Our results thus strongly indicate that the painted lady fulfils the oogenesis–flight syndrome, as migration is concentrated in its relatively short prereproductive period. Field data also showed a high positive correlation between mating frequency and host plant abundance, which suggests that mated females are able to locate potential breeding areas. This, together with the high fecundity estimated in laboratory trials, makes the painted lady a highly successful migratory insect.
Article
Prologue Part I: Evolutionary explanation Demography: age and stage structure Quantitative genetics and reaction norms Trade-offs Lineage-specific effects Part II: Age and size at maturity Number and size of offspring Reproductive lifespan and ageing Appendices Glossary References Author index Subject index.
Article
Myriad tiny insect species take to the air to engage in windborne migration, but entomology also has its 'charismatic megafauna' of butterflies, large moths, dragonflies and locusts. The spectacular migrations of large day-flying insects have long fascinated humankind, and since the advent of radar entomology much has been revealed about high-altitude night-time insect migrations. Over the last decade, there have been significant advances in insect migration research, which we review here. In particular, we highlight: (1) notable improvements in our understanding of lepidopteran navigation strategies, including the hitherto unsuspected capabilities of high-altitude migrants to select favourable winds and orientate adaptively, (2) progress in unravelling the neuronal mechanisms underlying sun compass orientation and in identifying the genetic complex underpinning key traits associated with migration behaviour and performance in the monarch butterfly, and (3) improvements in our knowledge of the multifaceted interactions between disease agents and insect migrants, in terms of direct effects on migration success and pathogen spread, and indirect effects on the evolution of migratory systems. We conclude by highlighting the progress that can be made through inter-phyla comparisons, and identify future research areas that will enhance our understanding of insect migration strategies within an eco-evolutionary perspective. © 2015 John Wiley & Sons Ltd/CNRS.
Article
The relationship between the energy expended per offspring, fitness of offspring, and parental fitness is presented in a two-dimensional graphical model. The validity of the model in determining an optimal parental strategy is demonstrated analytically. The model applies under various conditions of parental care and sibling care for the offspring but is most useful for species that produce numerous small offspring which are given no parental care.
Article
Density, photoperiod, and temperature exert profound effects on the life history and population growth of Oncopeltus. High temperature, long photoperiod, and low density result in earlier onset of reproduction, negatively skewed egg curves, and hence greater rates of population increase. Values or r (intrinsic rate of natural increase) vary from .0861 on a 16-hr day at 27⚬C with density of 10 pairs per container to .0369 on a 12-hr day at 23⚬C and 20 pairs. When r is low, length of life increases in partial compensation for suppressed reproduction. Photoperiod and density exert their influence only after adult eclosion, while temperature acts directly at all stages of life history to regulate the rate of development. The population responses of the phenotype to the environmental parameters studied are positive adaptations for a migrant insect such as Oncopeltus. It enters an essentially empty universe in the spring, when day length is increasing and temperatures are rising. The fact that all these factors...
Article
Long-range, seasonal migration is a widespread phenomenon among insects, allowing them to track and exploit abundant but ephemeral resources over vast geographical areas. However, the basic patterns of how species shift across multiple locations and seasons are unknown in most cases, even though migrant species comprise an important component of the temperate-zone biota. The painted lady butterfly Vanessa cardui is such an example; a cosmopolitan continuously-brooded species which migrates each year between Africa and Europe, sometimes in enormous numbers. The migration of 2009 was one of the most impressive recorded, and thousands of observations were collected through citizen science programmes and systematic entomological surveys, such as high altitude insect-monitoring radar and ground-based butterfly monitoring schemes. Here we use V. cardui as a model species to better understand insect migration in the Western Palaearctic, and we capitalise on the complementary data sources available for this iconic butterfly. The migratory cycle in this species involves six generations, encompassing a latitudinal shift of thousands of kilometres (up to 60 degrees of latitude). The cycle comprises an annual poleward advance of the populations in spring followed by an equatorward return movement in autumn, with returning individuals potentially flying thousands of kilometres. We show that many long-distance migrants take advantage of favourable winds, moving downwind at high elevation (from some tens of metres from the ground to altitudes over 1000 m), pointing at strong similarities in the flight strategies used by V. cardui and other migrant Lepidoptera. Our results reveal the highly successful strategy that has evolved in these insects, and provide a useful framework for a better understanding of long-distance seasonal migration in the temperate regions worldwide.
Article
1. Regulation of adult reproductive diapause and seasonal polyphenism was studied in two populations of the comma butterfly, Polygonia c-album (L.) (Nymphalidae), from Stockholm, Sweden, and Oxford, England. 2. In the univoltine Stockholm population short and long constant day-lengths (in the range 12–22 h) at 20°C were ineffective in averting the production of the dark, generally diapausing, morph, but the non-diapausing light morph could be produced if daylengths were increased during larval development. The procedure was especially effective with increases from 12 to 22 h, but the tendency was the same with a more realistic increase, from 18 to 20 h. 3. In the partially bivoltine English population a critical constant day-length for morph and diapause induction was found between 12 and 18 h. Decreasing daylengths above the critical daylength early or late in larval development resulted in production of the diapausing morph. 4. These results suggest a system for environmental control where day-lengths which increase throughout the larval period indicate an early date before summer solstice, meaning that there is sufficient time for a second generation of offspring to reach the hibernating adult stage before winter. The ecological significance of the results is discussed.
Article
1. The migrant Vanessa atalanta (L.) occurs throughout Europe and North Africa. In autumn, populations emigrate from northern and central Europe to the Mediterranean region to overwinter. In the spring, the northern range is recolonised by migrants from the south. The dynamics of the species in the winter range is poorly known. 2. From 1994 to 1999, adults and immatures of V. atalanta were monitored all year round in Mediterranean habitats in north-east Spain. 3. Data showed that the Catalonia lowlands is an area to which V. atalanta migrates to breed during the winter. Migrants arrive in October and early November and initiate a period of intensive breeding. Larval development occurs throughout the winter until a first annual generation of adults appears in early spring. 4. Most of the butterflies emerging in the spring emigrate and leave the area without breeding. The data suggest strongly that recolonisation of the northern range is by these butterflies not by wintering adults. Altitudinal migration also seems to be a common phenomenon, allowing a further summer generation of adults to occur at high elevations within the Mediterranean region. 5. The complex phenology of V. atalanta in its southern range has evolved as a strategy to track larval resources through space and time. Autumn migration coincides with the greatest availability of the main food plant, Urtica dioica L. Late spring migration occurs by the time food quality is decreasing.
Article
1. Effects of larval reserves and nutrients received as adults on fecundity and lifespan in female Danaus plexippus (the Monarch Butterfly) were measured to determine the relative importance of different sources of nutrients for reproduction and somatic maintenance. 2. Egg-laying lifespan was correlated with female size but not with the amount of male-derived nutrients or adult food concentration. 3. Lifetime fecundity was higher when females received a large first spermatophore, but was not affected by female size when lifespan was controlled or by adult food concentration. 4. At the end of their lives, females contained unlaid eggs and retained, on average, 88% of their initial mass. This proportion was unchanged in two years, although mean egg-laying lifespan varied from 22·5 to 28·7 days. 5. Egg mass decreased over the female lifespan, and was correlated with female size. 6. These results suggest that larval reserves are more important for somatic maintenance than adult income, but that the protein-rich nutrients received from males contribute to egg production. This supports theoretical predictions and empirical studies of other Lepidoptera showing that larval reserves are less likely to affect fecundity when the adult income can contribute substantially to egg production.
Article
This volume is divided into four parts. Part one consists of an introduction to migration and methods for its study. The second part examines proximate factors in migration: migration, winds and currents; physiology of migration; biomechanical and bioenergetic constraints on migration; and orientation and navigation. Part three examines migratory life histories and their evolution: seasonal migrations; migration to special habitats; migration under ephemeral conditions; behavioural variability in migration; polymorphisms and polyphenisms; and evolutionary genetics of migration. The final part discusses applications and implications in terms of pest management and conservation. -S.R.Harris
Developmental trade-offs in a polyphonic butterfy: lifespan versus reproduction
  • B Karlsson
  • F Stjernholm
  • C Wiklund
Karlsson, B., Stjernholm, F. & Wiklund, C. (2008) Developmental trade-offs in a polyphonic butterfy: lifespan versus reproduction. Functional Ecology, 22, 121-126.
Overwintering of the Red Admiral butterfly (Vanessa atalanta (L.)) on Howth Peninsula, Co. Dublin
  • Smyth F.
Butterflies of Europe
  • T Lafrancis
Lafrancis, T. (2004) Butterflies of Europe. Paris: Diatheo.
World distribution of the Vanessa cardui group (Nymphalidae)
  • Shields O.
The butterflies of Britain and Ireland
  • J. Thomas
  • R. Lewington
Delayed reproduction and fitness in variable environments
  • J Thomas
  • R Lewington
Thomas, J. & Lewington, R. (2010) The butterflies of Britain and Ireland. Gillingham: British Wildlife Publishing Tuljakulpar, S. (1990) Delayed reproduction and fitness in variable environments. Proceedings of the National Academy of Sciences of the United States of America, 87, 1139-1143.
World distribution of the Vanessa cardui group (Nymphalidae)
  • D A Roff
Roff, D.A. (1993) The evolution of life histories. London: Chapman and Hall. Shields, O. (1992) World distribution of the Vanessa cardui group (Nymphalidae). Journal of the Lepidopterists' Society, 46, 235-238.
Overwintering of the Red Admiral butterfly (Vanessa atalanta (L.)) on Howth Peninsula
  • F Smyth
  • D W Nash
Smyth, F. & Nash, D.W. (2008) Overwintering of the Red Admiral butterfly (Vanessa atalanta (L.)) on Howth Peninsula, Co. Dublin. The Irish Naturalists' Journal, 29, 81-86.