Sexual dimorphism and plasticity in wing shape in three Diptera

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Abstract

The ability of powered flight in insects facilitated their great evolutionary success allowing them to occupy various ecological niches. Beyond this primary task, wings are often involved in various premating behaviors, such as the generation of courtship songs and the initiation of mating in flight. These specific functions imply special adaptations of wing morphology, as well as sex-specific wing morphologies. Although wing morphology has been extensively studied in Drosophila melanogaster , a comprehensive understa nding of sexual wing shape dimorphisms and developmental plasticity is missing for other Diptera. Therefore, we raised flies of the three Diptera species Drosophila melanogaster, Ceratitis capitata and Musca domestica at different environmental conditions and applied geometric morphometrics to analyze wing shape. Our data showed extensive interspecific differences in wing shape, as well as a clear sexual wing shape dimorphism in all three species. We revealed an impact of different rearing temperatures wing shape in all three species, which was mostly explained by plasticity in wing size in D. melanogaster . Rearing densities had significant effects on allometric wing shape in D. melanogaster , while no obvious effects were observed for the other two species. Additionally, we do not find evidence for sex-specific response to different rearing conditions in all three species. We determined species-specific and common trends in shape alterations, and we hypothesize developmental and functional implications of our data.

Contribution to the Field Statement

The size and shape of organisms and organs must be tightly controlled during development to ensure proper functionality. However, morphological traits vary considerably in nature contributing to phenotypic diversity. Such variation can be the result of evolutionary adaptations as well as plasticity for example as reaction to changing environmental conditions during development. It is therefore a major aim in Biology to unravel the processes that control differences in adult morphology. Insect wings are excellent models to study how organ size and shape evolves because they facilitate basic tasks such as mating and feeding. Accordingly, a tremendous variety of wings sizes and shapes evolved in nature. Additionally, plasticity in wing morphology in response to different rearing conditions has been observed in many insects contributing to phenotypic diversity. In this work we applied Geometric Morphometrics to study wing shape in the three Diptera species: the Mediterranean fruit fly Ceratitis capitata , the Vinegar fly Drosophila melanogaster and the housefly Musca domestica . Flies were raised in different temperature and density regimes that allowed us to study the effects of these environmental factors on wing shape. Additionally, in accordance with different mating behaviors of these flies, we observed a clear sexual shape dimorphism in all three species. Since the three studied species represent serious pests and disease vectors, our findings may contribute to existing and future monitoring efforts.

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  1. SciScore for 10.1101/135749: (What is this?)

    Please note, not all rigor criteria are appropriate for all manuscripts.

    Table 1: Rigor

    NIH rigor criteria are not applicable to paper type.

    Table 2: Resources

    Experimental Models: Organisms/Strains
    SentencesResources
    We used the highly inbred laboratory strain Drosophila melanogaster w1118, which was kept at 18°C on standard food (400 g of malt extract, 400 g of corn flour, 50 g of soy flour, 110 g of sugar beet syrup, 51 g of agar, 90 g of yeast extract, 31.5 ml of propionic acid and 7.5 g of Nipagin dissolved in 40 ml of Ethanol, water up to 5 l).
    w1118
    suggested: None
    Software and Algorithms
    SentencesResources
    Intraspecific sexual dimorphism and effects of rearing conditions: Since most of the variation in shape was explained by differences between species (see Results), we split the analysis to further evaluate the effects of sex, rearing temperature, and density as well as potential interactions on wing shape within each species using Procrustes ANOVA in Geomorph (v. 3.3.1) (TableS2).
    Geomorph
    suggested: (geomorph, RRID:SCR_016482)
    Magnitudes of sexual shape dimorphism were estimated using the Discriminant Function Analysis (DFA) and expressed in units of Procrustes distance using MorphoJ (version 1.06d).
    MorphoJ
    suggested: (MorphoJ, RRID:SCR_016483)

    Results from OddPub: Thank you for sharing your code.


    Results from LimitationRecognizer: We detected the following sentences addressing limitations in the study:
    However, despite these technical and analytical limitations, we could show that the three factors contributed additively to the observed shape variation and we confirmed that the size correction indeed removed the effect of centroid size on wing shape variation. Therefore, we are convinced that we could observe general trends, which will be briefly discussed separately for each factor. Sexual dimorphism: We observed a clear sexual shape dimorphism in all three species. While mostly wing width differed between females and males in C. capitata and D. melanogaster, the most obvious sexual differences in M. domestica was in wing length. According to a clear impact of sex on wing size (Siomava et al., 2016) (Fig. S2), we found a clear contribution of the allometric component to the shape difference between males and females in D. melanogaster. For instance, a shift of CuA1 along the wing margin as also described by (Bitner-Mathé and Klaczko, 1999), we could only detect when the allometric component was included. In general, exclusion of the allometric coefficient decreased the sexual shape dimorphism, suggesting that most of the observed shape differences could be explained by differences in wing size. In contrast, sex had only a minor effect on wing size in C. capitata and M. domestica (Siomava et al., 2016) (Fig. S2). Accordingly, the impact of the allometric component on wing shape was weak. For instance, the variation in the wing length that was explained by the allometric com...

    Results from TrialIdentifier: No clinical trial numbers were referenced.


    Results from Barzooka: We did not find any issues relating to the usage of bar graphs.


    Results from JetFighter: We did not find any issues relating to colormaps.


    Results from rtransparent:
    • Thank you for including a conflict of interest statement. Authors are encouraged to include this statement when submitting to a journal.
    • Thank you for including a funding statement. Authors are encouraged to include this statement when submitting to a journal.
    • No protocol registration statement was detected.

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