What are the costs of learning? Modest trade-offs and constitutive costs do not set the price of fast associative learning ability in a parasitoid wasp.

Learning ability has been associated with energetic costs that typically become apparent through trade-offs in a wide range of developmental, physiological, and life-history traits. Costs associated with learning ability can be either constitutive or induced, depending on whether they are always incurred or only when information is actively learned and memorized. Using lines of the parasitoid wasp Nasonia vitripennis that were selected for fast associative learning ability, we assessed a range of traits that have previously been identified as potential costs associated with learning. No difference in longevity, lipid reserves, tibia length, egg load, or fecundity was observed between the selected and control lines. All of these traits are considered to potentially lead to constitutive costs in the setup of this study. A gradual reversal to baseline learning after two forms of relaxed selection was indicative of a small constitutive cost of learning ability. We also tested for a trade-off with other memory types formed at later stages, but found no evidence that the mid-term memory that was selected for caused a decrease in performance of other memory types. In conclusion, we observe only one minor effect of a constitutive cost and none of the other costs and trade-offs that are reported in the literature to be of significant value in this case. We, therefore, argue for better inclusion of ecological and economic costs in studies on costs and benefits of learning ability.

Regulatory and sequence evolution in response to selection for improved associative learning ability in Nasonia vitripennis.

BACKGROUND: Selection acts on the phenotype, yet only the genotype is inherited. While both the phenotypic and genotypic response to short-term selection can be measured, the link between these is a major unsolved problem in evolutionary biology, in particular for complex behavioural phenotypes. RESULTS: Here we characterize the genomic and the transcriptomic basis of associative learning ability in the parasitic wasp Nasonia vitripennis and use gene network analysis to link the two. We artificially selected for improved associative learning ability in four independent pairs of lines and identified signatures of selection across the genome. Allele frequency diverged consistently between the selected and control lines in 118 single nucleotide polymorphisms (SNPs), clustering in 51 distinct genomic regions containing 128 genes. The majority of SNPs were found in regulatory regions, suggesting a potential role for gene expression evolution. We therefore sequenced the transcriptomes of selected and control lines and identified 36 consistently differentially expressed transcripts with large changes in expression. None of the differentially expressed genes also showed sequence divergence as a result of selection. Instead, gene network analysis showed many of the genes with consistent allele frequency differences and all of the differentially expressed genes to cluster in a single co-expression network. At a functional level, both genomic and transcriptomic analyses implicated members of gene networks known to be involved in neural plasticity and cognitive processes. CONCLUSIONS: Taken together, our results reveal how specific cognitive abilities can readily respond to selection via a complex interplay between regulatory and sequence evolution.

Selection for associative learning of color stimuli reveals correlated evolution of this learning ability across multiple stimuli and rewards.

We are only starting to understand how variation in cognitive ability can result from local adaptations to environmental conditions. A major question in this regard is to what extent selection on cognitive ability in a specific context affects that ability in general through correlated evolution. To address this question, we performed artificial selection on visual associative learning in female Nasonia vitripennis wasps. Using appetitive conditioning in which a visual stimulus was offered in association with a host reward, the ability to learn visual associations was enhanced within 10 generations of selection. To test for correlated evolution affecting this form of learning, the ability to readily form learned associations in females was also tested using an olfactory instead of a visual stimulus in the appetitive conditioning. Additionally, we assessed whether the improved associative learning ability was expressed across sexes by color-conditioning males with a mating reward. Both females and males from the selected lines consistently demonstrated an increased associative learning ability compared to the control lines, independent of learning context or conditioned stimulus. No difference in relative volume of brain neuropils was detected between the selected and control lines.

Synergistic effect of daily temperature fluctuations and matching light-dark cycle enhances population growth and synchronizes oviposition behavior in a soil arthropod.

Some major aspects of insect life, like development time and reproduction, can benefit from fluctuating temperatures rather than a constant temperature regime. The benefit of fluctuating temperature has generally been attributed to the non-linear properties of the relationship of many life history traits with temperature. Daily temperature rise, however, usually coincide with the light phase of the photoperiodic cycle and there could be a benefit in linking daily temperature fluctuations with light and dark phases e.g. to anticipate the change in temperature. Such synergistic effects have primarily been studied in the light of activity patterns and gene expression, but have not yet been shown to extend to population dynamics and aspects of individual fitness like oviposition behavior. We therefore explored possible synergistic effects on life history traits of the springtail Orchesella cincta. We first test the primary effect of ecologically relevant temperature fluctuations of different amplitudes on population growth and total population mass. The slowest population growth was observed in the constant temperature regime treatment and the highest population growth in the regime with high amplitude fluctuations. In a second experiment, population growth and oviposition rhythm were measured under four different regimes; a constant light and temperature regime, thermoperiod only, photoperiod only and thermoperiod and photoperiod aligned as under natural conditions. The regime in which thermoperiod was aligned with photoperiod resulted in a higher population growth than could be realized by either factor alone. Also, significantly fewer eggs were laid in the constant temperature/light regime than in the other three regimes, strongly suggesting that this regime is stressful to O. cincta. Additionally, the fraction of eggs laid at night was highest in the regime with the combined temperature and light cycle. In conclusion, our results show that under these experimental conditions there is a synergistic effect of daily temperature fluctuations in combination with light/dark phases that can considerably influence important life history traits and affect behavior. Such effects are likely to be relevant under natural conditions.

Variation in reaction norms: Statistical considerations and biological interpretation.

Analysis of reaction norms, the functions by which the phenotype produced by a given genotype depends on the environment, is critical to studying many aspects of phenotypic evolution. Different techniques are available for quantifying different aspects of reaction norm variation. We examine what biological inferences can be drawn from some of the more readily applicable analyses for studying reaction norms. We adopt a strongly biologically motivated view, but draw on statistical theory to highlight strengths and drawbacks of different techniques. In particular, consideration of some formal statistical theory leads to revision of some recently, and forcefully, advocated opinions on reaction norm analysis. We clarify what simple analysis of the slope between mean phenotype in two environments can tell us about reaction norms, explore the conditions under which polynomial regression can provide robust inferences about reaction norm shape, and explore how different existing approaches may be used to draw inferences about variation in reaction norm shape. We show how mixed model-based approaches can provide more robust inferences than more commonly used multistep statistical approaches, and derive new metrics of the relative importance of variation in reaction norm intercepts, slopes, and curvatures.

Extending the integrated phenotype: covariance and correlation in plasticity of behavioural traits.

In the field of behavioural ecology there has been a longstanding interest in the evolution of phenotypic plasticity, as plasticity in behavioural traits such as foraging, mating, and reproduction governs the capacity of organisms to cope with environmental variability. In this paper we highlight the need for an integrated perspective to phenotypic plasticity of traits, taking into account covariation among plastic responses of traits. We discuss new perspectives on the importance of integrated plasticity of traits for adaptive behavioural strategies. We review empirical evidence for correlated plasticity across behavioural traits in insects, for example, through genetic correlation, a shared pool of resources or dependency on a common developmental path. Taking on an integrated plasticity perspective, we suggest an alternative explanation for the apparent lack of costs of plasticity, and offer a better understanding of the relative benefits of plasticity or canalization of traits.

Measuring the plasticity of developmental rate across insect populations: comment on Rocha and Klaczko (2012).

Rocha and Klaczko emphasize the general complexity of reaction norm shape and caution that ignoring such complexity can be misleading when forcing nonlinear reaction norms into linear shapes. They refer to our article on differences in plasticity of Drosophila serrata populations along a latitudinal gradient as an example of a misleading simplifying approach. However, their claim that an artifact is introduced into our analyses by calculating developmental rate as the reciprocal of development time (rate = time(-1)) is based on a misunderstanding of the mathematical properties of the thermal developmental rate reaction norm. Here we discuss why developmental rate is a suitable measure for our study and under which circumstances it is appropriate to describe developmental rate by a linear model.

Plasticity versus environmental canalization: population differences in thermal responses along a latitudinal gradient in Drosophila serrata.

The phenotypic plasticity of traits, defined as the ability of a genotype to express different phenotypic values of the trait across a range of environments, can vary between habitats depending on levels of temporal and spatial heterogeneity. Other traits can be insensitive to environmental perturbations and show environmental canalization. We tested levels of phenotypic plasticity in diverse Drosophila serrata populations along a latitudinal cline ranging from a temperate, variable climate to a tropical, stable climate by measuring developmental rate and size-related traits at three temperatures (16 degrees C, 22 degrees C, and 28 degrees C). We then compared the slopes of the thermal reaction norms among populations. The 16-22 degrees C part of the reaction norms for developmental rate was flatter (more canalized) for the temperate populations than for the tropical populations. However, slopes for the reaction norms of the two morphological traits (wing size, wing:thorax ratio), were steeper (more plastic) in the temperate versus the tropical populations over the entire thermal range. The different latitudinal patterns in plasticity for developmental rate and the morphological traits may reflect contrasting selection pressures along the tropical-temperate thermal gradient.