How frequently are insects wounded in the wild? A case study using Drosophila melanogaster

Abstract

Wounding occurs across multicellular organisms. Wounds can affect host mobility and reproduction, with ecological consequences for competitive interactions and predator-prey dynamics. Wounds are also entry points for pathogens. An immune response is activated upon injury, resulting in the deposition of the brown-black pigment melanin in insects. Despite the abundance of immunity studies in the laboratory and the potential ecological and evolutionary implications of wounding, the prevalence of wounding in wild-collected insects is rarely systematically explored. We investigated the prevalence and potential causes of wounds in wild-collected Drosophilidae flies. We found that 31% of Drosophila melanogaster were wounded or damaged. The abdomen was the most frequently wounded body part, and females were more likely to have melanized patches on the ventral abdomen, compared with males. Encapsulated parasitoid egg frequency was approximately 10%, and just under 1% of Drosophilidae species had attached mites, which also caused wounds. Wounding is prevalent in D. melanogaster, likely exerting selection pressure on host immunity for two reasons: on a rapid and efficient wound repair and on responding efficiently to opportunistic infections. Wounding is thus expected to be an important driver of immune system evolution and to affect individual fitness and population dynamics.

Keywords: cuticle damage; cuticle injury; cuticle wound; melanin; mite; wild-collected organism.

Figure 1.

Examples of wounding and damage in D. melanogaster. Arrows indicate melanized areas likely resulting from an immune response or missing parts of the wings. Wild-collected flies with damage to the (a) head, (b) thorax, (c) leg, (d) wing, (e,f) ventral abdomen. Images from labratory-reared flies under controlled mating conditions to illustrate (g) wounds on the female vaginal furcal dorsolateral fold (formerly termed lateral folds in [44], more recent terminology from [47]) resulting from mating and (h) a virgin female without copulatory wounds. The sex of each fly is indicated at the top right of each image. Images (g,h) taken by A. Finsterbusch.

Figure 2.

Frequency of wounding in wild-collected D. melanogaster. (a) The proportion of flies with none, one or two or more damage locations, (b) the proportion of flies with wounds to the external cuticle (HLTA: head, legs, thorax and abdomen), (c) the proportion of females and males showing HLTA wounding, (d–f) the proportion of the flies with total, ventral and dorsal abdominal melanized spots by sex (for a–f, n = 1174), (g) the proportion of flies with wing damage (total) and damage that is either to a vein or not to a vein (n = 338), and (h) the proportion of females showing copulatory wounding according to collection site (n = 163). Stars indicate statistically significant differences where: **p <0.001 and ***p <0.0001. The grey-shaded areas of the cartoon flies show the area of damage in each panel.

Figure 3.

Melanized encapsulated parasitoid eggs in wild-collected D. melanogaster. Images of melanized encapsulated parasitoid eggs in (a) the head, (b) the thorax and abdomen, and (c) the abdomen, (d) the proportion of flies with parasitoids by season and site and (e) the proportion of flies with one or more encapsulated parasitoids (for d, n = 1174 flies were examined). ES: early summer, LS: late summer and A: autumn. The asterisk indicates p < 0.05 and the line indicates the significant post hoc difference between the early summer Lindicke site and the late summer Gartenbau site.

Figure 4.

Mites found on wild-collected Drosophilidae. (a) Mite load across all flies, (b) Macrocheles sp. attached to a female D. melanogaster, (c) a Pergamasus sp. attached to a D. subobscura, (d) the numbers of mites attached to different body parts. The bristles were on the head and the thorax. One fly had morphologically similar mites attached to the ventral abdomen and to the dorsal thorax, and another fly was found with mites attached to the ventral and the dorsal abdomen. The melanized areas visible on the abdomen of (e) a male D. melanogaster and (f) a female D. melanogaster, after removing the mites. For (a,d), n = 56.

Figure 5.

µCT and SEM of mites attached to Drosophilidae. (a–c) Scaptomyza pallida with attached mites whose chelicerae appear to slightly penetrate the dorsal abdominal cuticle and (d) where a mite- or fly-derived substance (orange) is visible at the contact point. (e–h) Two smaller mites attached to the dorsal side of a D. melanogaster or D. simulans female dorsal abdomen. (i–p) Two D. melanogaster or D. simulans females with a single large mite attached to (i–l) the ventral or (m–p) dorsal side of the abdomen, grasping a cuticular fold (green) with the chelicerae (yellow) and pedipalps (blue). Scale bars indicate 500 µm if not otherwise indicated. Mite species are unidentified.