Mating opportunity and the evolution of sex-specific mortality rates in a butterfly

Life history theory predicts that organisms should only invest resources into intrinsic components of life span to the degree that it pays off in terms of reproductive success. Here, we investigate if the temporal distribution of mating opportunities may have influenced the evolution of intrinsic mortality rates in the butterfly Pararge aegeria (Satyrinae). In this species, females mate only once and the frequency of male mating opportunities depends on the temporal emergence pattern of virgin females. As expected, in a population from Madeira where females emerge continuously throughout the year, there was no sex difference in adult life span, while in a Swedish population with synchronised female emergence, males had significantly shorter life spans compared to females. A logistic mortality model provided the best fit to the observed change in age-specific mortality and all categories reached an asymptotic mortality rate of a similar magnitude. However, the Swedish males reached this mortality plateau more rapidly than the other categories. External mortality, due to water and food limitation, affected the pattern of sex-specific mortality but males from Sweden still had higher rates of mortality compared to all other categories. We argue that selection on male longevity is likely to be weaker in Sweden because under synchronised emergence, all females emerge and mate within a short period of time, after which male reproductive value will quickly approach zero. On Madeira, however, male reproductive value decrease more slowly with age since the probability of finding a receptive female is constant over the year. Received: 29 July 1999 / Accepted: 23 August 1999     

Hostplants and classification: a review of nymphalid butterflies

In reviewing the hostplant associations of nymphalid butterflies, particular emphasis is placed on the intractable problem of nymphalid classification. Although offering few certain conclusions, if used in conjunction with more formal morphological characters, the data presented should contribute toward a resolution of the inter-relationships of the many widely recognized groupings within the Nymphalidae, several of which seem to be broadly characterized by typical host families. As a direct result of this analysis, the presumed association between larval hostplants and unpalatability is re-appraised.     

Nettle-feeding nymphalid butterflies: temperature, development and distribution

1. Four nymphalid butterflies, Aglais urticae L., Inachis io L., Polygonia c-album L. and Vanessa atalanta L., share the same primary host plant, Urtica dioica L., but have different margins to their U.K. and European ranges. Their developmental responses to a series of constant temperatures were measured.
2. Degree-day requirements were found broadly to explain the relative distributions and differences in voltinism of A. urticae , P. c-album and I. io . The migrant V. atalanta did not fit into the predicted pattern, and this species may be more limited by its ability to overwinter.
3. Although the most northerly distributed species, A. urticae , had the lowest degree-day requirement, it had the highest developmental threshold and performed best (for mortality, pupal weight and relative growth rate) at high experimental temperatures. It is suggested that this may be due to the gregarious nature of its larvae and their possible ability to thermoregulate.
4. At southern margins, different distributional limits may be explained partly by larval gregariousness (a more northern trait) and maximum temperatures at which development is possible.
5. Limits to the distributions of these mobile species are at least partially explicable by the interaction of climatic patterns and thermal biology. A rapid response to climate change is predicted, and has already been observed in two of the species.     

Worldwide variation in life-span sexual dimorphism and sex-specific environmental mortality rates

In all human populations mean life span of women generally exceeds that of men, but the extent of this sexual dimorphism varies across different regions of the world. Our purpose here is to study, using global demographic and environmental data, the general tendency of this variation and local deviations from it. We used data on male and female life history traits and environmental conditions for 227 countries and autonomous territories; for each country or territory the life-span dimorphism was defined as the difference between mean life spans of women and men. The general tendency is an increase of life-span dimorphism with increasing average male-female life span; this tendency can be explained using a demographic model based on the Makeham-Gompertz equation. Roughly, the life-span dimorphism increases with the average life span because of an increase in the duration of expressing sex- and age-dependent mortality described by the second (exponential) term of the Makeham-Gompertz equation. Thus we investigated the differences in male and female environmental mortality described by the first term of the Makeham-Gompertz equation fitted to the data. The general pattern that resulted was an increase in male mortality at the highest and lowest latitudes. One plausible explanation is that specific factors tied to extreme latitudes influence males more strongly than females. In particular, alcohol consumption increases with increasing latitude and, on the contrary, infection pressures increase with decreasing latitude. This finding agrees with other observations, such as an increase in male mortality excess in Europe and Christian countries and an increase in female mortality excess in Asia and Muslim countries. An increase in the excess of female mortality may also be due to increased maternal mortality caused by an increase in fertility. However, this relation is not linear: In regions with the highest fertility (e.g., in Africa) the excess of female mortality is smaller than in regions with relatively lower fertility (e.g., in Asia). A possible explanation of this phenomenon is an evolutionary adaptation of women to the pressures of extremely high fertility by means of some reduction of their maternal mortality.     

Identification of feeding attractants in oak sap for adults of two nymphalid butterflies, Kaniska canace and Vanessa indica

The active compounds of oak‐sap odour in attracting adults of two butterflies, Kaniska canace (L.) and Vanessa indica (Herbst) (Lepidoptera: Nymphalidae), were identified by chemical analyses, electroantennogram (EAG) and two behavioural assays: proboscis extension reflex (PER) and attraction to artificial tree models. Fourteen compounds were identified from two sap samples collected in 1997 and 1998, of which the major volatiles were ethanol and acetic acid (≈ 900 p.p.m. and 500 p.p.m. in sap, respectively). However, the chemical composition of the minor volatiles varied considerably between the two samples. Among 13 chemicals tested, V. indica showed strong PER to five aliphatic acids (acetic, propionic, butyric, isobutyric and isovaleric), 2‐methylpropan‐1‐ol and 3‐hydroxybutan‐2‐one, whereas the PER‐active compounds for K. canace were these seven compounds and also ethanol, 3‐methylbutan‐1‐ol and 1‐hydroxypropan‐2‐one. In two‐choice behavioural bioassays, the model scented with a sap‐odour mimic, which was an aqueous mixture of the PER‐active compounds, was more attractive to the two butterflies than an unscented control. These results demonstrated that the sap odour stimulates foraging behaviour of the butterfly. Although EAG responses of both butterflies to 3‐methylbutan‐1‐ol and that of V. indica to 2‐methylpropan‐1‐ol were positively dose‐dependent, responses to other compounds were not strong and not dose‐dependent at 1–100 μg doses. These EAG responsiveness suggests that the olfactory receptors for these compounds might be few in the antenna and that the butterflies have enough olfactory sensitivity to the dose of 1 μg.     

Anatomy of the oral valve in nymphalid butterflies and a functional model for fluid uptake in Lepidoptera

The food canal of the proboscis of Lepidoptera serves for the uptake of nutrient fluids and the discharge of saliva. A valve was discovered at the entrance to the sucking pump in the head that separates these countercurrent flows in nymphalid butterflies. Three species of Nymphalidae were examined by dissections and light microscopic serial semithin sections. The sucking pump is a unit composed of three structures: (1) the oral valve, which is a projection of the epipharynx extending into the anterior cibarial lumen, (2) the expandable lumen, and (3) the posterior sphincter valve which controls influx into the oesophagus. Based on the microanatomical results, a functional model is presented to account for the uptake and swallowing of fluids and for the control of the salivary flow into the food canal of the proboscis. Dilator muscles of the sucking pump expand the lumen by pulling on the muscular dorso-anterior side. This opens the oral valve and fluid can be drawn into the lumen from the food canal of the proboscis. Circular compressor muscles which attach to both sides of the sclerotized ventro-posterior wall of the sucking pump reduce the size of the lumen; passively they close the oral valve and press fluid through the relaxed posterior sphincter opening into the oesophagus. According to this model saliva can be discharged into the food canal during the swallowing phase. The oral valve and pumping unit are similar in all studied species despite the fact that saliva presumably plays a special role in the derived pollen-feeding behaviour of one of them, viz. Heliconius melpomene.     

Mating system shifts and transposable element evolution in the plant genus Capsella

Background

Despite having predominately deleterious fitness effects, transposable elements (TEs) are major constituents of eukaryote genomes in general and of plant genomes in particular. Although the proportion of the genome made up of TEs varies at least four-fold across plants, the relative importance of the evolutionary forces shaping variation in TE abundance and distributions across taxa remains unclear. Under several theoretical models, mating system plays an important role in governing the evolutionary dynamics of TEs. Here, we use the recently sequenced Capsella rubella reference genome and short-read whole genome sequencing of multiple individuals to quantify abundance, genome distributions, and population frequencies of TEs in three recently diverged species of differing mating system, two self-compatible species (C. rubella and C. orientalis) and their self-incompatible outcrossing relative, C. grandiflora.

Results

We detect different dynamics of TE evolution in our two self-compatible species; C. rubella shows a small increase in transposon copy number, while C. orientalis shows a substantial decrease relative to C. grandiflora. The direction of this change in copy number is genome wide and consistent across transposon classes. For insertions near genes, however, we detect the highest abundances in C. grandiflora. Finally, we also find differences in the population frequency distributions across the three species.

Conclusion

Overall, our results suggest that the evolution of selfing may have different effects on TE evolution on a short and on a long timescale. Moreover, cross-species comparisons of transposon abundance are sensitive to reference genome bias, and efforts to control for this bias are key when making comparisons across species.

Electronic supplementary material

The online version of this article (doi:10.1186/1471-2164-15-602) contains supplementary material, which is available to authorized users.     

Protandry and postandry in two related butterflies: conflicting evidence about sex-specific trade-offs between adult size and emergence time

Natural selection acting on timing of metamorphosis can be sex-specific, resulting in differences in timing between males and females. Insects with discrete generations frequently show protandry: males usually mature before females. Both Euphydryas editha and E. aurinia butterflies followed this trend. The present study was motivated by the unusual observation of consistent postandry in addition to protandry. In a single E. editha population observed over 20 years the emergence period of males was longer than that of females, both the first and last emerging individuals being males. Variance of timing among individual E. editha larvae is imposed by spatial patchiness of the snowmelt that releases them from winter diapause. If individual larvae released late from diapause were to compensate for their lateness by shortening their development times, they would be small at maturity. If such compensation were only partial, they would be both late and small. Size and timing would become associated. If females were more prone to such partial compensation than males, the observations of postandry could be explained and the prediction made that any tendency for late individuals to be small should be stronger in females than in males. This was the case: in 1 year late males were the same size as early males, in a second year they were larger. Late females were significantly smaller than early females in both years. In E. aurinia, results were opposite both to theoretical prediction and to the observations from E. editha: although the male emergence period was longer than that of females exactly as in E. editha, late males were smaller than early ones, while late females were not small. The data from E. editha support the hypothesis of a sex-specific trade-off between size and emergence time, the data from E. aurinia do not.     

DNA barcoding of nymphalid butterflies (Nymphalidae: Lepidoptera) from Western Ghats of India

We have checked the utility of DNA barcoding for species identification of nymphalid butterflies from Western Ghats of India by using 650 bp sequence of mitochondrial gene cytochrome c oxidase subunit I. Distinct DNA barcoding gap (i.e. difference between intraspecies and interspecies nucleotide divergence), exists between species studied here. When our sequences were compared with the sequences of the conspecifics submitted from different geographic regions, nine cases of deep intraspecies nucleotide divergences were observed. In spite of this, NJ (Neighbour Joining) clustering analysis successfully discriminated all species. Observed cases of deep intraspecies nucleotide divergences certainly warrant further study.     

Latitude and rates of diversification in birds and butterflies

Central to many explanations of latitudinal diversity gradients is the idea that rates of species diversification increase towards the equator. However, there have been few explicit tests of whether or not this pattern exists. Using sister-group analyses to compare 48 clades of passerine birds and swallowtail butterflies from different latitudes, I found evidence that relative rates of diversification per unit time are indeed higher towards the equator. This pattern is explicable in terms of abiotic factors which vary continuously with latitude, and may be further enhanced by diversity-dependent speciation and extinction processes.     

Mating system and recombination affect molecular evolution in four Triticeae species.

Mating systems and recombination are thought to have a deep impact on the organization and evolution of genomes. Because of the decline in effective population size and the interference between linked loci, the efficacy of selection is expected to be reduced in regions with low recombination rates and in the whole genome of self-fertilizing species. At the molecular level, relaxed selection is expected to result in changes in the rate of protein evolution and the pattern of codon bias. It is increasingly recognized that recombination also affects non-selective processes such as the biased gene conversion towards GC alleles (bGC). Like selection, this kind of meiotic drive in favour of GC over AT alleles is expected to be reduced in weakly recombining regions and genomes. Here, we investigated the effect of mating system and recombination on molecular evolution in four Triticeae species: two outcrossers (Secale cereale and Aegilops speltoides) and two selfers (Triticum urartu and Triticum monococcum). We found that GC content, possibly driven by bGC, is affected by mating system and recombination as theoretically predicted. Selection efficacy, however, is only weakly affected by mating system and recombination. We investigated the possible reasons for this discrepancy. A surprising one is that, in outcrossing lineages, selection efficacy could be reduced because of high substitution rates in favour of GC alleles. Outcrossers, but not selfers, would thus suffer from a 'GC-induced' genetic load. This result sheds new light on the evolution of mating systems.     

The evolution of sex-specific grandparental harm

Recent empirical studies indicate that grandparents favour some categories of grandchildren over others. Here, we expand the previous theoretical foundation for this finding and show that grandchild-harming phenotypes are predicted to evolve by ‘sexually antagonistic zygotic drive (SA-zygotic drive) of the sex chromosomes’. We use the logic of Hamilton''s rule to develop a new ‘no-cost-to-self nepotism rule’ that greatly simplifies the determination of the invasion criteria for mutations that cause grandparents to harm grandchildren. We use this theory to generate predictions that distinguish SA-zygotic drive from theory based solely on paternity assurance. The major diagnostic prediction is that grandmothers, and to a lesser degree grandfathers, will evolve grandson-harming phenotypes that reduce the level of sib competition experienced by their more closely related granddaughters, especially in their sons'' families. This prediction is supported by data from recent studies showing (i) grandmothers invest more in granddaughters than grandsons, and counterintuitively, (ii) paternal grandmothers reduce the survival of their grandsons. We conclude that SA-zygotic drive is plausibly operating in humans via sexually antagonistic grandparental care.     

The evolution of sex-specific immune defences

Why do males and females often differ in their ability to cope with infection? Beyond physiological mechanisms, it has recently been proposed that life-history theory could explain immune differences from an adaptive point of view in relation to sex-specific reproductive strategies. However, a point often overlooked is that the benefits of immunity, and possibly the costs, depend not only on the host genotype but also on the presence and the phenotype of pathogens. To address this issue we developed an adaptive dynamic model that includes host–pathogen population dynamics and host sexual reproduction. Our model predicts that, although different reproductive strategies, following Bateman''s principle, are not enough to select for different levels of immunity, males and females respond differently to further changes in the characteristics of either sex. For example, if males are more exposed to infection than females (e.g. for behavioural reasons), it is possible to see them evolve lower immunocompetence than females. This and other counterintuitive results highlight the importance of ecological feedbacks in the evolution of immune defences. While this study focuses on sex-specific natural selection, it could easily be extended to include sexual selection and thus help to understand the interplay between the two processes.     

Behavioural trade-offs between growth and mortality explain evolution of submaximal growth rates

1. The importance of body size and growth rate in ecological interactions is widely recognized, and both are frequently used as surrogates for fitness. However, if there are significant costs associated with rapid growth rates then its fitness benefits may be questioned. 2. In replicated whole-lake experiments, we show that a domestic strain of rainbow trout (artificially selected for maximum intrinsic growth rate) use productive but risky habitats more than wild trout. Consequently, domestic trout grow faster in all situations, experience greater survival in the absence of predators, but have lower survival in the presence of predators. Therefore, rapid growth rates are selected against due to increased foraging effort (or conversely, lower antipredator behaviour) that increases vulnerability to predators. In other words, there is a behaviourally mediated trade-off between growth and mortality rates. 3. Whereas rapid growth is beneficial in many ecological interactions, our results show the mortality costs of achieving it are large in the presence of predators, which can help explain the absence of an average phenotype with maximized growth rates in nature.     

Mating positions and the evolution of asymmetric insect genitalia

Genital asymmetry is a recurring phenomenon in insect morphology and current data suggest that it has arisen multiple times independently in several neopteran orders. Various explanations have been proposed, including space constraints, ecological constraints, sexual selection via antagonistic coevolution, and sexual selection via changed mating positions. Each of these hypotheses may best explain individual cases, but only the last seems to account for the large majority of insect genital asymmetries. Here I summarize the basic assumptions and evolutionary steps implied in this model and review the evidence for each of them. Several components of this scenario can be easily tested, for example by including genital asymmetries and mating positions in phylogenetic analyses. Others require in-depth analyses of the function of asymmetric genital structures, targeted comparative analyses (e.g., of taxa with sex-role reversal, taxa with reversal to symmetry, etc.), and of female genital neuroanatomy.     

Mating systems and sexual division of foraging effort affect puddling behaviour by butterflies

Abstract. 1. Foraging effort can vary among age classes and between the sexes. In many Lepidoptera, young males feed from mud, dung or carrion in a behaviour known as 'puddling', whereas females rarely puddle. In at least one species, males transfer sodium gained from puddling to females at mating for use in egg production.
2. Here we examine sex- and age-specific puddling patterns in seven montane butterfly species. We also test the hypothesis that among species in which young males predominate at puddles, differences in age- and sex-specific puddling patterns for a given species are related to mean female lifetime mating numbers.
3. For five species, young males fed proportionately more at puddles than other sex and age classes. Two species showed anomalous feeding patterns. In one, young females predominated at puddles; in the other, butterflies were rarely found at flowers.
4. As predicted, among the five species in which young males feed proportionately more at puddles, mean number of lifetime matings by females was negatively correlated with frequency of mud puddling by older females. A second prediction that mean number of lifetime matings by females is positively correlated with frequency of mud puddling by older males was not supported.
5. The results provide support for interspecific variation in division of responsibility between the sexes for resource acquisition for female reproduction, indicating close coordination between the sexes of foraging and life-history tactics.     

Color pattern analysis of nymphalid butterfly wings: revision of the nymphalid groundplan

To better understand the developmental mechanisms of color pattern variation in butterfly wings, it is important to construct an accurate representation of pattern elements, known as the "nymphalid groundplan". However, some aspects of the current groundplan remain elusive. Here, I examined wing-wide elemental patterns of various nymphalid butterflies and confirmed that wing-wide color patterns are composed of the border, central, and basal symmetry systems. The central and basal symmetry systems can express circular patterns resembling eyespots, indicating that these systems have developmental mechanisms similar to those of the border symmetry system. The wing root band commonly occurs as a distinct symmetry system independent from the basal symmetry system. In addition, the marginal and submarginal bands are likely generated as a single system, referred to as the "marginal band system". Background spaces between two symmetry systems are sometimes light in coloration and can produce white bands, contributing significantly to color pattern diversity. When an element is enlarged with a pale central area, a visually similar (yet developmentally distinct) white band is produced. Based on the symmetric relationships of elements, I propose that both the central and border symmetry systems are comprised of "core elements" (the discal spot and the border ocelli, respectively) and a pair of "paracore elements" (the distal and proximal bands and the parafocal elements, respectively). Both core and paracore elements can be doubled, or outlined. Developmentally, this system configuration is consistent with the induction model, but not with the concentration gradient model for positional information.