EB Ford revisited: assessing the long-term stability of wing-spot patterns and population genetic structure of the meadow brown butterfly on the Isles of Scilly

This is the author accepted manuscript. The final version is available from the publisher via the DOI in this record.Data files of wing spot sizes and AFLP genotypes available from the Dryad Digital Repository: http://dx.doi.org/10.5061/dryad.j7v42.Understanding selection in the wild remains a major aim of evolutionary ecology and work by Ford and colleagues on the meadow brown butterfly Maniola jurtina did much to ignite this agenda. A great deal of their work was conducted during the 1950s on the Isles of Scilly. They documented island-specific wing-spot patterns that remained consistent over about a decade, but patterns on some islands changed after environmental perturbation. It was suggested that these wing-spot patterns reflected island-specific selection and that there was little migration between islands. However, genetic studies to test the underlying assumption of restricted migration are lacking and it is also unknown whether the originally described wing-spot patterns have persisted over time. We therefore collected female butterflies from five of Ford's original study locations, including three large islands (St Mary's, St Martin's and Tresco) and two small islands (Tean and St Helen's). Wing-spot patterns had not changed appreciably over time on three of the islands (two large and one small), but were significantly different on the other two. Furthermore, analysis of 176 amplified fragment length polymorphisms revealed significant genome-wide differentiation among the five islands. Our findings are consistent with Ford's conclusions that despite the close proximity of these islands, there is restricted gene flow among them.Heredity advance online publication, 2 November 2016; doi:10.1038/hdy.2016.94.We thank the Genetics Society for a fieldwork grant (to DJH) that funded the collection trip and DJH thanks Mike Johnson for sparking interest in this area. SWB is supported by the Australian Research Council and a Ramsay Fellowship, NW by a Royal Society Wolfson Fellowship and NERC and DJH by the Leverhulme Trust

The combined effect of two mutations that alter serially homologous color pattern elements on the fore and hindwings of a butterfly

<p>Abstract</p> <p>Background</p> <p>The ability for serially homologous structures to acquire a separate identity has been primarily investigated for structures dependent on Hox gene input but is still incompletely understood in other systems. The fore and hindwings of butterflies are serially homologous structures as are the serially homologous eyespots that can decorate each of these wings. Eyespots can vary in number between fore and hindwings of the same individual and mutations of large effect can control the total number of eyespots that each of the wings displays. Here we investigate the genetics of a new spontaneous color pattern mutation, <it>Missing</it>, that alters eyespot number in the nymphalid butterfly, <it>Bicyclus anynana</it>. We further test the interaction of <it>Missing </it>with a previously described mutation, <it>Spotty</it>, describe the developmental stage affected by <it>Missing</it>, and test whether <it>Missing </it>is a mutant variant of the gene <it>Distal-less </it>via a linkage association study.</p> <p>Results</p> <p><it>Missing </it>removes or greatly reduces the size of two of the hindwing eyespots from the row of seven eyespots, with no detectable effect on the rest of the wing pattern. Offspring carrying a single <it>Missing </it>allele display intermediate sized eyespots at these positions. <it>Spotty </it>has the opposite effect of <it>Missing</it>, i.e., it introduces two extra eyespots in homologous wing positions to those affected by <it>Missing</it>, but on the forewing. When <it>Missing </it>is combined with <it>Spotty </it>the size of the two forewing eyespots decreases but the size of the hindwing spots stays the same, suggesting that these two mutations have a combined effect on the forewing such that <it>Missing </it>reduces eyespot size when in the presence of a <it>Spotty </it>mutant allele, but that <it>Spotty </it>has no effect on the hindwing. <it>Missing </it>prevents the complete differentiation of two of the eyespot foci on the hindwing. We found no evidence for any linkage between the <it>Distal-less </it>and <it>Missing </it>genes.</p> <p>Conclusion</p> <p>The spontaneous mutation <it>Missing </it>controls the differentiation of the signaling centers of a subset of the serial homologous eyespots present on both the fore and the hindwing in a dose-dependent fashion. The effect of <it>Missing </it>on the forewing, however, is only observed when the mutation <it>Spotty </it>introduces additional eyespots on this wing. <it>Spotty</it>, on the other hand, controls the differentiation of eyespot centers only on the forewing. <it>Spotty</it>, unlike <it>Missing</it>, may be under Ubx gene regulation, since it affects a subset of eyespots on only one of the serially homologous wings.</p

What are the effects of maternal and pre-adult environments on ageing in humans, and are there lessons from animal models?

An open issue in research on ageing is the extent to which responses to the environment during development can influence variability in life span in animals, and the health profile of the elderly in human populations. Both affluence and adversity in human societies have profound impacts on survivorship curves, and some of this effect may be traceable to effects in utero or in infancy. The Barker Hypothesis that links caloric restriction in very early life to disruptions of glucose-insulin metabolism in later life has attracted much attention, as well as some controversy, in medical circles. It is only rarely considered by evolutionary biologists working on phenotypic plasticity, or by biogerontologists studying model organisms such as C. elegans or Drosophila. One crucial mechanism by which animals can respond in an adaptive manner to adverse conditions, for example in nutrition or infection, during development is phenotypic plasticity. Here we begin with a discussion of adaptive plasticity in animals before asking what such phenomena may reveal of relevance to rates of ageing in animals, and in humans. We survey the evidence for effects on adult ageing of environmental conditions during development across mammalian and invertebrate model organisms, and ask whether evolutionary conserved mechanisms might be involved. We conclude that the Barker Hypothesis is poorly supported and argue that more work in human populations should be integrated with multi-disciplinary studies of ageing-related phenomena in experimental populations of different model species that are subjected to nutritional challenges or infections during pre-adult development

Molecular evolution of HoxA13 and the multiple origins of limbless morphologies in amphibians and reptiles

Developmental processes and their results, morphological characters, are inherited through transmission of genes regulating development. While there is ample evidence that cis-regulatory elements tend to be modular, with sequence segments dedicated to different roles, the situation for proteins is less clear, being particularly complex for transcription factors with multiple functions. Some motifs mediating protein-protein interactions may be exclusive to particular developmental roles, but it is also possible that motifs are mostly shared among different processes. Here we focus on HoxA13, a protein essential for limb development. We asked whether the HoxA13 amino acid sequence evolved similarly in three limbless clades: Gymnophiona, Amphisbaenia and Serpentes. We explored variation in ω (dN/dS) using a maximum-likelihood framework and HoxA13sequences from 47 species. Comparisons of evolutionary models provided low ω global values and no evidence that HoxA13 experienced relaxed selection in limbless clades. Branch-site models failed to detect evidence for positive selection acting on any site along branches of Amphisbaena and Gymnophiona, while three sites were identified in Serpentes. Examination of alignments did not reveal consistent sequence differences between limbed and limbless species. We conclude that HoxA13 has no modules exclusive to limb development, which may be explained by its involvement in multiple developmental processes

A model for selection of eyespots on butterfly wings

The development of eyespots on the wing surface of butterflies of the family Nympalidae is one of the most studied examples of biological pattern formation.However, little is known about the mechanism that determines the number and precise locations of eyespots on the wing. Eyespots develop around signaling centers, called foci, that are located equidistant from wing veins along the midline of a wing cell (an area bounded by veins). A fundamental question that remains unsolved is, why a certain wing cell develops an eyespot, while other wing cells do not. We illustrate that the key to understanding focus point selection may be in the venation system of the wing disc. Our main hypothesis is that changes in morphogen concentration along the proximal boundary veins of wing cells govern focus point selection. Based on previous studies, we focus on a spatially two-dimensional reaction-diffusion system model posed in the interior of each wing cell that describes the formation of focus points. Using finite element based numerical simulations, we demonstrate that variation in the proximal boundary condition is sufficient to robustly select whether an eyespot focus point forms in otherwise identical wing cells. We also illustrate that this behavior is robust to small perturbations in the parameters and geometry and moderate levels of noise. Hence, we suggest that an anterior-posterior pattern of morphogen concentration along the proximal vein may be the main determinant of the distribution of focus points on the wing surface. In order to complete our model, we propose a two stage reaction-diffusion system model, in which an one-dimensional surface reaction-diffusion system, posed on the proximal vein, generates the morphogen concentrations that act as non-homogeneous Dirichlet (i.e., fixed) boundary conditions for the two-dimensional reaction-diffusion model posed in the wing cells. The two-stage model appears capable of generating focus point distributions observed in nature. We therefore conclude that changes in the proximal boundary conditions are sufficient to explain the empirically observed distribution of eyespot focus points on the entire wing surface. The model predicts, subject to experimental verification, that the source strength of the activator at the proximal boundary should be lower in wing cells in which focus points form than in those that lack focus points. The model suggests that the number and locations of eyespot foci on the wing disc could be largely controlled by two kinds of gradients along two different directions, that is, the first one is the gradient in spatially varying parameters such as the reaction rate along the anterior-posterior direction on the proximal boundary of the wing cells, and the second one is the gradient in source values of the activator along the veins in the proximal-distal direction of the wing cell

Marginal Eyespots on Butterfly Wings Deflect Bird Attacks Under Low Light Intensities with UV Wavelengths

Predators preferentially attack vital body parts to avoid prey escape. Consequently, prey adaptations that make predators attack less crucial body parts are expected to evolve. Marginal eyespots on butterfly wings have long been thought to have this deflective, but hitherto undemonstrated function.Here we report that a butterfly, Lopinga achine, with broad-spectrum reflective white scales in its marginal eyespot pupils deceives a generalist avian predator, the blue tit, to attack the marginal eyespots, but only under particular conditions-in our experiments, low light intensities with a prominent UV component. Under high light intensity conditions with a similar UV component, and at low light intensities without UV, blue tits directed attacks towards the butterfly head.In nature, birds typically forage intensively at early dawn, when the light environment shifts to shorter wavelengths, and the contrast between the eyespot pupils and the background increases. Among butterflies, deflecting attacks is likely to be particularly important at dawn when low ambient temperatures make escape by flight impossible, and when insectivorous birds typically initiate another day's search for food. Our finding that the deflective function of eyespots is highly dependent on the ambient light environment helps explain why previous attempts have provided little support for the deflective role of marginal eyespots, and we hypothesize that the mechanism that we have discovered in our experiments in a laboratory setting may function also in nature when birds forage on resting butterflies under low light intensities

Genomic Sequence around Butterfly Wing Development Genes: Annotation and Comparative Analysis

, where a whole-genome BAC library allows targeted access to large genomic regions. genes. Comparative analysis with orthologous regions of the lepidopteran reference genome allowed assessment of conservation of fine-scale synteny (with detection of new inversions and translocations) and of DNA sequence (with detection of high levels of conservation of non-coding regions around some, but not all, developmental genes)., both involved in multiple developmental processes including wing pattern formation