Empirical studies of sexual selection typically focus on one of the two mechanisms of sexual selection without integrating these into a description of total sexual selection, or study total sexual selection without quantifying the contributions of all of the mechanisms of sexual selection. However, this can provide an incomplete or misleading view of how sexually selected traits evolve if the mechanisms of sexual selection are opposing or differ in form. Here, we take a two‐fold approach to advocate a direction for future studies of sexual selection. We first show how a quantitative partitioning and examination of sexual selection mechanisms can inform by identifying illustrative studies that describe both male–male competition and female mate choice acting on the same trait. In our sample, the most common trait where this occurred was body size, and selection was typically linear. We found that male–male competition and female mate choice can be reinforcing or opposing, although the former is most common in the literature. The mechanisms of sexual selection can occur simultaneously or sequentially, and we found they were more likely to be opposing when the mechanisms operated sequentially. The degree and timing that these mechanisms interact have important implications for the operation of sexual selection and needs to be considered in designing studies. Our examples highlight where empirical data are needed. We especially lack standardized measures of the form and strength of selection imposed by each mechanism of sexual selection and how they combine to determine total sexual selection. Secondly, using quantitative genetic principles, we outline how the selection imposed by individual mechanisms can be measured and combined to estimate the total strength and form of sexual selection. We discuss the evolutionary consequences of combining the mechanisms of sexual selection and interpreting total sexual selection. We suggest how this approach may result in empirical progress in the field of sexual selection.
Butterfly wing patterns provide a rich comparative framework to study how morphological complexity develops and evolves. Here we used CRISPR/Cas9 somatic mutagenesis to test a patterning role for , a signaling ligand gene previously identified as a hotspot of shape-tuning alleles involved in wing mimicry. We show that loss-of-function causes multiple modifications of pattern elements in seven nymphalid butterfly species. In three butterflies with a conserved wing-pattern arrangement, is necessary for the induction of stripe-like patterns known as symmetry systems and acquired a novel eyespot activator role specific to forewings. In two species, specifies the boundaries between melanic fields and the light-color patterns that they contour. In the passionvine butterfly , removal shows opposite effects on adjacent pattern elements, revealing a dual role across the wing field. Finally, acquired a divergent role in the patterning of interveinous patterns in the monarch, a basal nymphalid butterfly that lacks stripe-like symmetry systems. These results identify as an instructive signal for the prepatterning of a biological system of exuberant diversity and illustrate how shifts in the deployment and effects of a single developmental gene underlie morphological change.
A striking diversity of compound eye size and shape has evolved among insects. The number of ommatidia and their size are major determinants of the visual sensitivity and acuity of the compound eye. Each ommatidium is composed of eight photoreceptor cells that facilitate the discrimination of different colours via the expression of various light sensitive Rhodopsin proteins. It follows that variation in eye size, shape, and opsin composition is likely to directly influence vision. We analyzed variation in these three traits in D. melanogaster, D. simulans and D. mauritiana. We show that D. mauritiana generally has larger eyes than its sibling species, which is due to a combination of larger ommatidia and more ommatidia. In addition, intra- and inter-specific differences in eye size among D. simulans and D. melanogaster strains are mainly caused by variation in ommatidia number. By applying a geometric morphometrics approach to assess whether the formation of larger eyes influences other parts of the head capsule, we found that an increase in eye size is associated with a reduction in the adjacent face cuticle. Our shape analysis also demonstrates that D. mauritiana eyes are specifically enlarged in the dorsal region. Intriguingly, this dorsal enlargement is associated with enhanced expression of rhodopsin 3 in D. mauritiana. In summary, our data suggests that the morphology and functional properties of the compound eyes vary considerably within and among these closely related Drosophila species and may be part of coordinated morphological changes affecting the head capsule.
The nature of developmental buffering processes has been debated extensively, based on both theoretical reasoning and empirical studies. In particular, controversy has focused on the question of whether distinct processes are responsible for canalization, the buffering against environmental or genetic variation, and for developmental stability, the buffering against random variation intrinsic in developmental processes. Here, we address this question for the size and shape of Drosophila melanogaster wings in an experimental design with extensively replicated and fully controlled genotypes. The amounts of variation among individuals and of fluctuating asymmetry differ markedly among genotypes, demonstrating a clear genetic basis for size and shape variability. For wing shape, there is a high correlation between the amounts of variation among individuals and fluctuating asymmetry, which indicates a correspondence between the two types of buffering. Likewise, the multivariate patterns of shape variation among individuals and of fluctuating asymmetry show a close association. For wing size, however, the amounts of individual variation and fluctuating asymmetry are not correlated. There was a significant link between the amounts of variation between wing size and shape, more so for fluctuating asymmetry than for variation among individuals. Overall, these experiments indicate a considerable degree of shared control of individual variation and fluctuating asymmetry, although it appears to differ between traits.
This study examines the causes of emigration from small fragments of suitable habitat in a species that has a distinct metapopulation structure, frequent turnover of local populations, and substantial migration among local populations and currently unoccupied habitat fragments. We conducted a field experiment in which 727 individuals of the Glanville fritillary butterfly (Melitaea cinxia) originating from four regions were marked and released simultaneously in a natural environment. In three of the four source regions, larvae for the experiment were collected from dozens of small local populations, some of which had been established in the previous summer (new populations), whereas the remaining populations were older. In two of the source regions, female butterflies prefer a host plant (Veronica spicata) that is not present in the release area, where there is only Plantago lanceolata, the preferred host plant of females from the other two source regions. We found that migration rate of males was unrelated to any of the factors studied in this experiment. In contrast, two factors influenced the migration rate of females. First, Veronica‐preferring females had higher emigration rate than Plantago‐preferring females from the Plantago‐containing release patches, demonstrating that the individual perception of habitat quality significantly influences the migration rate of females. Second, females from newly‐established populations were more dispersive than females from older populations, supporting the notion that metapopulation processes (recurrent colonizations) select for increased migration. The observed migration rate was not correlated with any body size measurements, and thus the observed differences in migration rate were apparently caused by differences in the behaviour of female butterflies rather than in their flight capacity.
Gene duplications within the conserved Hox cluster are rare in animal evolution, but in Lepidoptera an array of divergent Hox-related genes (Shx genes) has been reported between pb and zen. Here, we use genome sequencing of five lepidopteran species (Polygonia c-album, Pararge aegeria, Callimorpha dominula, Cameraria ohridella, Hepialus sylvina) plus a caddisfly outgroup (Glyphotaelius pellucidus) to trace the evolution of the lepidopteran Shx genes. We demonstrate that Shx genes originated by tandem duplication of zen early in the evolution of large clade Ditrysia; Shx are not found in a caddisfly and a member of the basally diverging Hepialidae (swift moths). Four distinct Shx genes were generated early in ditrysian evolution, and were stably retained in all descendent Lepidoptera except the silkmoth which has additional duplications. Despite extensive sequence divergence, molecular modelling indicates that all four Shx genes have the potential to encode stable homeodomains. The four Shx genes have distinct spatiotemporal expression patterns in early development of the Speckled Wood butterfly (Pararge aegeria), with ShxC demarcating the future sites of extraembryonic tissue formation via strikingly localised maternal RNA in the oocyte. All four genes are also expressed in presumptive serosal cells, prior to the onset of zen expression. Lepidopteran Shx genes represent an unusual example of Hox cluster expansion and integration of novel genes into ancient developmental regulatory networks.
BackgroundButterflies are popular model organisms to study physiological mechanisms underlying variability in oogenesis and egg provisioning in response to environmental conditions. Nothing is known, however, about; the developmental mechanisms governing butterfly oogenesis, how polarity in the oocyte is established, or which particular maternal effect genes regulate early embryogenesis. To gain insights into these developmental mechanisms and to identify the conserved and divergent aspects of butterfly oogenesis, we analysed a de novo ovarian transcriptome of the Speckled Wood butterfly Pararge aegeria (L.), and compared the results with known model organisms such as Drosophila melanogaster and Bombyx mori.ResultsA total of 17306 contigs were annotated, with 30% possibly novel or highly divergent sequences observed. Pararge aegeria females expressed 74.5% of the genes that are known to be essential for D. melanogaster oogenesis. We discuss the genes involved in all aspects of oogenesis, including vitellogenesis and choriogenesis, plus those implicated in hormonal control of oogenesis and transgenerational hormonal effects in great detail. Compared to other insects, a number of significant differences were observed in; the genes involved in stem cell maintenance and differentiation in the germarium, establishment of oocyte polarity, and in several aspects of maternal regulation of zygotic development.ConclusionsThis study provides valuable resources to investigate a number of divergent aspects of butterfly oogenesis requiring further research. In order to fully unscramble butterfly oogenesis, we also now also have the resources to investigate expression patterns of oogenesis genes under a range of environmental conditions, and to establish their function.
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