Genetic Variation and the Role of Insect Life History Traits in the Ability of Drosophila Larvae to Develop in the Presence of a Competing Filamentous Fungus

Abstract

Competitive interactions between organisms from distantly related phylogenetical branches have been suggested as being one of the most pervasive forms of interspecific competition. However, so-called inter-kingdom competition has rarely been the focus of ecological and evolutionary studies. Thus, a relatively novel hypothesis has been proposed on the basis that saprophagous insects might intensively compete with filamentous fungi for ephemeral resources (e.g. decaying plant tissue). Consideration that life history traits (e.g. developmental time) are adaptive in determining developmental success in the presence of con-or hetero-specifics competitors implies that these traits have been progressively established by natural selection. Because a similar scenario may apply to antagonistic interactions between saprophagous insects and filamentous fungi, one can expect the existence of heritable variation in developmental success when insect larvae are forced to grow in the presence of noxious mould. Therefore, this study aimed at discovering whether a local population of Drosophila melanogaster indeed harbours genetic variation in developmental success in the presence of the mould Aspergillus niger. By using the isofemale line technique, single larvae forced to feed on fungal infected or uninfected substrate were analysed for variation in survival probability to the adult stage, developmental time and body size of emerged adults. I found genetic variation in survival probability in fungal infected substrates but not in uninfected larval food sources. Mean developmental time and body size varied significantly among isofemale lines in both types of larval environment. Survival was negatively correlated with developmental time on fungal infected substrate, but variation in developmental time on fungalfree substrates was not correlated with survival on fungal infected food patches. Within-trait correlation between fungal infected and uninfected substrates was surprisingly weak, and developmental time was not correlated with body size. The results of this study demonstrate (a) the existence of genetic variation for larval developmental success in the presence of A. niger in a Drosophila population, and (b) heritability of important insect life history traits differed as a function of the larval environment (fungal infected or uninfected feeding substrate). I discuss models that might explain heritability differences and the evolutionary consequences of these results.

Predatory cannibalism in Drosophila melanogaster larvae

“…There is also some evidence from several Drosophila species that the larvae can be nutritionally limited for growth and survival [42][43][44] , especially those hatching from eggs laid late, after the food patch has already been colonized for some time 45 . Desiccation or colonization of the food source by inedible and possibly toxic microorganisms 46 means that such latecomer larvae may face deterioration of their food source even if larval density is low; this would enhance the incentive to cannibalize conspecifics more advanced in their development. Furthermore, in addition to energy and protein, cannibalized conspecifics may be a source of limiting elements such as sodium 7 , which is scarce in fruits.…”

Experimental evolution of resistance against a competing fungus in Drosophila melanogaster

“…If spatial and temporal variation in the degree to which insect breeding substrates are infested with fungi may be one explanation for the maintenance of genetic variation in this type of ecological interaction (Rohlfs 2006), we may expect that adaptation to a fungus-contaminated environment resulting in increased mould resistance reduces evolutionary Wtness in other traits (Gillespie and Turelli 1989;Fry 2003). In agreement with this prediction, Xies from selected populations had reduced resistance to desiccation, heat stress and starvation (though not cold stress).…”

“…Given that noxious fungi are ubiquitous on Drosophila breeding substrates, insects in natural populations are likely to be selected for resistance to microbial antagonists. Yet, substantial genetic variation in the ability of Drosophila melanogaster to successfully develop in fungus-infested breeding substrates has nevertheless been documented in natural populations, using the isofemale line technique (Rohlfs 2006). An increased rate at which infested patches are encountered by the insects over generations as well as an increasing degree of mould infestation may thus still shift the balance towards better performance in a mouldy environment.…”

“…They also enable the detection of Wtness trade-oVs related to the evolved trait through assays of correlated responses (Fry 2003). Genetically determined variation in survival of D. melanogaster larvae on mould-infested substrates ranging from less than 20% to nearly 100% (Rohlfs 2006) may indicate the existence of such trade-oVs in resistance to competing fungi.…”

Host–parasitoid interaction as affected by interkingdom competition

“…Rohlfs (&) Zoological Institute, Department of Animal Ecology, Christian-Albrechts-University of Kiel, Kiel, Germany e-mail: rohlfs@zoologie.uni-kiel.de and Mitchell 1997;Wertheim et al 2002;Rohlfs et al 2005;Rohlfs 2006); however, insect larvae can signiWcantly impair fungal growth, depending on the age of fungal colonies, fungus species and larval density (Hodge and Arthur 1997;Hodge et al 1999;Rohlfs 2005a;Rohlfs et al 2005). Saprophagous Drosophila melanogaster larvae may achieve suppression of mould growth by disrupting hyphae through group formation on fungal colonies (Rohlfs 2005b), with larger groups more successful at destroying mould than smaller groups or single larvae, eventually giving rise to an Allee eVect for larval development (Rohlfs et al 2005).…”