Anticipatory gene regulation driven by maternal effects in an insect–host system

Abstract

Adaptive mechanisms involved in the prediction of future environments are common in organisms experiencing temporally variable environments. One of these is AGR (anticipatory gene regulation); in which differential gene expression occur in an individual, triggered by the experience of an ancestor. In this study, we explored the existence of AGR driven by a maternal effect, in an insect–host system. We analyzed gene expression of detoxifying systems in aphids across two generations, by shifting mothers and offspring from chemically defended to nondefended hosts, and vice versa. Then, we measured fitness (intrinsic rate of increase) and the relative abundance of transcripts from certain candidate genes in daughters, using RT‐qPCR (quantitative reverse‐transcription PCR). We found AGR in most cases, but responses varied according to the system being analyzed. For some pathways (e.g., cathepsins), the experience of both mothers and offsprings affected the response (i.e., when both, mother and daughter grew in the defended host, the maximum response was elicited; when only the mother grew in the defended host, an intermediate response was elicited; and when both, mother and daughter grew in a nondefended host, the response was undetectable). In other cases (esterases and GSTs), gene over‐expression was maintained even if the daughter was transferred to the nondefended host. In spite of these changes at the gene‐regulatory level, fitness was constant across hosts, suggesting that insects keep adapted thanks to this fluctuating gene expression. Also, it seems that that telescopic reproduction permits aphids to anticipate stressful environments, by minute changes in the timing of differential gene expression.

Limited effects of the maternal rearing environment on the behaviour and fitness of an insect herbivore and its natural enemy

“…Aphids mostly have a parthenogenetic, telescopic reproduction strategy [10], meaning that every nymph is a clonal copy of the mother and that the mother’s fitness is a key determinant of offspring fitness [11]. Due to telescopic reproduction, aphid fitness can be influenced by grand-maternal as well as maternal experience, termed transgenerational plasticity, which could lead to complex maternal effects between aphid generations [7].…”

“…However, the direct effect of mother’s fitness is often stronger than the maternal host plant environment, as the maternal plant host environment of aphids does not always have an effect on offspring survival and fecundity of aphids, as seen in milkweed-oleander aphid ( Aphis nerii ) [11] and bird cherry oat aphid ( Rhopalosiphum padi ) [14]. Conversely, the fitness of Myzus persicae mother aphids did not differ when feeding on chemically defended and non-defended plant hosts, but their daughters were able to anticipate a stressful environment by modifying gene expression depending on the plant host that the mother fed on [10].…”

Proteomic profile of aphids exposed to wheat with different contents of benzoxazinoids

“…As described above (see Introduction), the exposure periods were selected considering the telescoping generations that characterize aphid biology (e.g. the progenies are influenced by maternal experience for up to three asexual generations) because two generations are sufficient to trigger an anticipatory response in aphids (Nespolo et al, 2015). By contrast, we selected four generations because this ensured a full response to the current host, excluding maternal effects.…”

“…Thus, in the present study, aphid proteomes are obtained after two generations of experience in each host, a period known to trigger short‐term anticipatory responses in aphids (e.g. gene expression) according to recent host experience (Nespolo et al ., ); the responses are also analyzed after four generations. This method ensures a pure within‐generation response to the current host, which is known to be vital for aphid rates (e.g.…”