Corresponding author: Jens Joschinski (
Academic editor:
Climate change is the largest challenge of the 21st century (
When climate change drives environmental parameters out of tolerable limits, survival is generally considered to depend on microevolution and phenotypic plasticity (
Bet-hedging is adaptive variance of phenotypes around an ‘optimal’ mean value that can buffer against unforeseen environments. For example, variability in seed germination ensures that not all seeds enter the vulnerable seedling stage at the same time, so dormant seeds can survive to the next year under adverse conditions (
Why is evidence for bet-hedging so scarce? On the one hand, the prevalence of bet-hedging might be underestimated due to the challenge of finding good evidence (
According to the conceptual framework, true costs of plasticity need to be separated from phenotype-environment mismatches. A plastic organism that is imperfectly matched to the environment is still better adapted than a canalized organism, which does not fit at all to one environment. Thus, mismatches with the environment represent the limit of an adaptive strategy, and cannot be considered true costs of plasticity. The real costs of phenotypic plasticity can then be split into global (maintenance) and local (production) costs. Maintenance costs are independent of the environment, and arise from the ability to be plastic
In accordance with the discussion on phenotypic plasticity, true costs of bet-hedging need to be separated from limits of the otherwise adaptive strategy: By inducing sub-optimal phenotypes, bet-hedging decreases the fitness in an average environment. This decrease in arithmetic mean fitness is not a true cost, but the core of the insurance strategy that increases fitness over longer times, i.e., geometric mean fitness (
Similar to costs of phenotypic plasticity, costs of bet-hedging can be split into global (maintenance) and local (production) costs. I hypothesize that maintenance costs manifest in a lower overall fitness, because bet-hedging requires a mechanism to generate variability. Bet-hedging could for example be achieved by high sensitivity to small environmental change (microplasticity), as has been observed in the response of seeds to germination conditions (
One possible bet-hedging mechanism is stochastic polyphenism, i.e. a stochastic choice of alternative phenotypes (
With this research idea I want to ask whether seasonal polyphenism is a bet-hedging strategy, and whether its evolution is hampered by fitness costs. I am looking for collaborations, as well as a working environment and research team for a postdoctoral project.
Aphids reproduce asexually over summer, and switch to production of sexual forms when the days shorten. The response to day length follows a logistic curve (Fig.
Below I propose one potential research plan for the main experiment. Methodology, choice of species and origin of aphid clones are all amendable to change, as they depend on the infrastructure and location of the host institute, on funding and on further collaborations. I first assume that I will collect
To obtain aphids with sufficiently different environmental and genetic backgrounds, I require aphid lines originating from a larger regional scale. Nevertheless, to compare the spread of reproductive mode switch in a single experiment, the different lines need to be induced at a similar mean (critical) day length, which correlates with latitude (
The experiment requires aphid lines from a gradient of winter unpredictability. This has been defined by
While the standard deviation in onset of winter can be easily calculated, it neglects adaptive phenotypic plasticity. For example, the response to day length is modulated by temperature (
The procedure for 12 clones kept at two day lengths is as follows (Fig.
When plotting the percentage of sexual offspring against day length, I will obtain a logistic curve as in Fig.
glmer (Induction ~ treatment * environment + (1 | mother/environment), family = binomial)
A significant interaction will support the hypothesis that the transient period correlates with environmental unpredictability. In addition, a significant positive effect of environment alone would indicate that clones from the most unpredictable environments also take riskier (later) strategies, as the modelling approach of
Bet-hedging could be achieved by two different modes: First, a single mother aphid can produce both sexual and asexual offspring. Secondly, each mother can produce only one type of offspring, but the choice of the type differs among genetically identical mothers. Literature suggests that mixed families exist in
Because photoperiodic induction requires rearing all offspring I will obtain detailed data on life-history traits. I hypothesize that clones which cope with high environmental unpredictability suffer from generally reduced fertility (maintenance costs), or from higher production costs when reared near the critical day length that induces transition from asexual to sexual reproduction (Fig.
Because development times and fecundity per day of the parent aphids are known, I construct life history tables and derive population growth based on a Leslie matrix, which gives a detailed account of aphid fitness (
For both dataset I will apply the model:
Fitness ~ day_length * environment + (1 | mother/environment)
A significant interaction of day length and environment is evidence for production costs (increased costs close to critical day length). If there is a significant effect of environment, this will be evidence for maintenance costs (generally reduced fitness).
Strong evidence for bet-hedging is provided by the observation that phenotypic variance can be quantitatively predicted by environmental variation (
Depending on host institute and collaborative projects, several details of the experiment can be adapted. Below I describe potential variations from the research plan.
Because polyphenism in reproductive modes is a primitive feature of the Aphidoidea (
The experiment requires aphid lines from several locations throughout Europe. I plan to sample aphid lines shortly before the experiments, because aphids can evolve quickly despite being asexual (
The experiment is logistically challenging. It requires frequently transferring aphids from 240 plants to new plants, and I need 1200 host plants in total. The procedure would be considerably easier, if the parent’s reproductive mode was known without having to rear all offspring. If the sexuality of the offspring could be determined on newly born nymphs, it would reduce the number of plants to 240 and reduce the time from 49 to 34 days. Thus, I would be happy for any suggestions to determine reproductive modes of young offspring morphologically.
In
I am looking for collaborators with knowledge in aphid biology and/or bet-hedging theory, and for a research environment that has at least two climate chambers and sufficient greenhouse space to rear about 1200 plants. The project will require approximately 3000€ to collect aphids, as well as small funds for aphid and plant rearing, and for student helpers for general maintenance of aphid clones and plants.
The proposed research project carries the danger that aphids do not hedge their bets, which makes an analysis of costs of bet-hedging obsolete. The phenotypic variance I want to assess has however also been observed in a single aphid clone before (
Preliminary work during my doctoral thesis (to be submitted in 2016) focused on the constrains of the sexual polyphenism. Aphids are generally considered to benefit from climate change by extending their phenology into early spring and late autumn. During the doctoral thesis I asked whether aphids can use the novel temperature-day length combinations efficiently. I demonstrated that aphids suffer fitness constraints under short days, so the evolution of phenology might be constrained (
I expect that the experiment outlined in this proposal will be the first to demonstrate a long-term fitness advantage of bet-hedging in insects. Furthermore, with the experiment I quantify the production costs and the maintenance costs of bet-hedging. I expect that the results of the experiment will be summarized in one publication (e.g. in American Naturalist or Evolution).
Depending on further collaborations, the main experiment could be supplemented by further studies. For example, I could assess the gene expression of aphids reared under the critical day length. The data could be used to study the switch in reproductive modes (photoperiodism), which would result in a further publication.
This research idea greatly benefitted from stimulating discussions within the DFG-funded collaborative research center “SFB 1047 insect timing”. I particularly thank Thomas Hovestadt, Oliver Mitesser, Christophe Gadenne and Jochen Krauss for helpful comments on the manuscript.
Funding was provided by the German Research Foundation (DFG), collaborative research center SFB 1047 “Insect timing",
Project C3.
The author declares no conflict of interest.
Funding was provided by the German Research Foundation (DFG), collaborative research center SFB 1047 “Insect timing",
Project C3.
The author declares no conflict of interest.
Map of Europe, with intended sampling location.