Precise Quantification of Behavioral Individuality From 80 Million Decisions Across 183,000 Flies.

Individual animals behave differently from each other. This variability is a component of personality and arises even when genetics and environment are held constant. Discovering the biological mechanisms underlying behavioral variability depends on efficiently measuring individual behavioral bias, a requirement that is facilitated by automated, high-throughput experiments. We compiled a large data set of individual locomotor behavior measures, acquired from over 183,000 fruit flies walking in Y-shaped mazes. With this data set we first conducted a "computational ethology natural history" study to quantify the distribution of individual behavioral biases with unprecedented precision and examine correlations between behavioral measures with high power. We discovered a slight, but highly significant, left-bias in spontaneous locomotor decision-making. We then used the data to evaluate standing hypotheses about biological mechanisms affecting behavioral variability, specifically: the neuromodulator serotonin and its precursor transporter, heterogametic sex, and temperature. We found a variety of significant effects associated with each of these mechanisms that were behavior-dependent. This indicates that the relationship between biological mechanisms and behavioral variability may be highly context dependent. Going forward, automation of behavioral experiments will likely be essential in teasing out the complex causality of individuality.

The effect of environmental enrichment on behavioral variability depends on genotype, behavior, and type of enrichment.

Non-genetic individuality in behavior, also termed intragenotypic variability, has been observed across many different organisms. A potential cause of intragenotypic variability is sensitivity to minute environmental differences during development, which are present even when major environmental parameters are kept constant. Animal enrichment paradigms often include the addition of environmental diversity, whether in the form of social interaction, novel objects or exploratory opportunities. Enrichment could plausibly affect intragenotypic variability in opposing ways: it could cause an increase in variability due to the increase in microenvironmental variation, or a decrease in variability due to elimination of aberrant behavior as animals are taken out of impoverished laboratory conditions. In order to test these hypothesis, we assayed five isogenic Drosophila melanogaster lines raised in control and mild enrichment conditions, and one isogenic line under both mild and intense enrichment conditions. We compared the mean and variability of six behavioral metrics between our enriched fly populations and the laboratory housing control. We found that enrichment often caused a small increase in variability across most of our behaviors, but that the ultimate effect of enrichment on both behavioral means and variabilities was highly dependent on genotype and its interaction with the particular enrichment treatment. Our results support previous work on enrichment that presents a highly variable picture of its effects on both behavior and physiology.

Alternative competition-induced digestive strategies yield equal growth, but constrain compensatory growth in red-eyed treefrog larvae.

Compensatory growth is well documented across taxa and provides a fitness advantage to animals who would otherwise reach a smaller reproductive size. We investigated the role of competition-induced gut plasticity in facilitating a compensatory response in red-eyed treefrog larvae. We reared larvae at low, medium, and high densities with different per capita resources, environments known to produce individuals with long and short guts. We then transferred larvae to competitively equal environments to determine if longer guts provided an advantage when resources became available. We predicted that larvae from higher densities with longer guts would exhibit hyperphagia and compensatory growth. We measured growth over 1-week, as well as the time to and size at metamorphosis. To assess mechanisms underlying the growth response, we measured diet transit time and intake. Growth, development, and metamorph snout-vent length did not differ between larvae with long and short guts. Instead, different gut lengths were associated with dramatically different feeding strategies. Medium- and high-density larvae fed at rates far below what their guts could accommodate. However, the combination of low intake and longer guts extended diet transit times, presumably increasing digestibility. This unexpected strategy achieved the same results as that of low-density larvae, which ate twice as much food, but passed it more quickly through a shorter gut. The lack of a compensatory response may be attributed to the costs of accelerated growth and weak seasonal time constraints in the tropics. This suggests that although compensatory growth is widespread among animals, expression of the response may vary with environmental context. J. Exp. Zool. 323A: 778-788, 2015. © 2015 Wiley Periodicals, Inc.

Behavioral idiosyncrasy reveals genetic control of phenotypic variability.

Quantitative genetics has primarily focused on describing genetic effects on trait means and largely ignored the effect of alternative alleles on trait variability, potentially missing an important axis of genetic variation contributing to phenotypic differences among individuals. To study the genetic effects on individual-to-individual phenotypic variability (or intragenotypic variability), we used Drosophila inbred lines and measured the spontaneous locomotor behavior of flies walking individually in Y-shaped mazes, focusing on variability in locomotor handedness, an assay optimized to measure variability. We discovered that some lines had consistently high levels of intragenotypic variability among individuals, whereas lines with low variability behaved as although they tossed a coin at each left/right turn decision. We demonstrate that the degree of variability is itself heritable. Using a genome-wide association study (GWAS) for the degree of intragenotypic variability as the phenotype across lines, we identified several genes expressed in the brain that affect variability in handedness without affecting the mean. One of these genes, Ten-a, implicates a neuropil in the central complex of the fly brain as influencing the magnitude of behavioral variability, a brain region involved in sensory integration and locomotor coordination. We validated these results using genetic deficiencies, null alleles, and inducible RNAi transgenes. Our study reveals the constellation of phenotypes that can arise from a single genotype and shows that different genetic backgrounds differ dramatically in their propensity for phenotypic variabililty. Because traditional mean-focused GWASs ignore the contribution of variability to overall phenotypic variation, current methods may miss important links between genotype and phenotype.