The emergence and development of behavioral individuality in clonal fish

Abstract

Behavioral individuality is a ubiquitous phenomenon in animal populations, yet the origins and developmental trajectories of individuality, especially very early in life, are still a black box. Using a high-resolution tracking system, we mapped the behavioral trajectories of genetically identical fish (Poecilia formosa), separated immediately after birth into identical environments, over the first 10 weeks of their life at 3 s resolution. We find that (i) strong behavioral individuality is present at the very first day after birth, (ii) behavioral differences at day 1 of life predict behavior up to at least 10 weeks later, and (iii) patterns of individuality strengthen gradually over developmental time. Our results establish a null model for how behavioral individuality can develop in the absence of genetic and environmental variation and provide experimental evidence that later-in-life individuality can be strongly shaped by factors pre-dating birth like maternal provisioning, epigenetics and pre-birth developmental stochasticity.

Fig. 1. Three stylized scenarios of how individuality can emerge.

Individuality might be present at birth (A) or emerge gradually (B) or in an abrupt fashion (C) after birth (see main text for details).

Fig. 2. Individuality is present at day one after birth and is not explained by differences in maternal identity or body size.

Repeatability of median swimming speed at hourly intervals on the first day after birth (A); each line represents one individual (N = 26). Maternal identity (B) did not explain variation in swimming speeds among individuals. Small and large points indicate the hourly (i.e. 11 data points per individual) and daily median swimming speeds, respectively, of individuals from each mother on day one after birth; see also Table 1. Behavior on day one after birth (C) was not related to an individual’s total length on their first day of life; see also Supplementary Table 3. Small and large points indicate hourly and daily median swimming speeds for each individual respectively; gray lines indicate posterior estimates for the effects of body size on behavior. Throughout, lines and points are colored according to the individual’s behavior in hour one on day one (yellow represents higher swimming speeds; purple indicates lower swimming speeds). Source Data are provided as a Source Data file.

Fig. 3. Individuality increases gradually throughout the first 70 days of development.

The predicted values of median individual swimming speed diverge over time (A) leading to gradual increases in the among-individual variance and hence repeatability (B) of behavior. These models included only the 26 individuals on which we had complete data for the first 10 weeks of life to ensure that absolute levels of variation would remain comparable over time. Individual lines in (A) are colored according to their predicted behavior in week 1 with yellow indicating greater swimming speeds and purple indicating lower swimming speeds. In (B), shown are the posterior modes of each variance estimate and its 95% CI. Source Data are provided as a Source Data file.

Fig. 4. Earlier-in-life individuality predict later-in-life individuality.

A Individual behavior was significantly positively correlated across all 10 weeks of observation. Each plot represents the among-individual correlation in behavior between two particular weeks in the ten-week experiment. The points in the plot represent the individual’s behavior for that week; throughout, individuals are colored according to their week 1 behavior where yellow represents greater swimming speeds and purple represents lower swimming speeds. The line on each plot is the estimated among-individual correlation between behavior in those two weeks; correlations were significant across all weeks. B Shown are the among-individual correlations between behavior in a given week and behavior 1, 2, 3, 4, or 5 weeks later. The correlations with behavior 2–5 weeks later have significantly steeper slopes than the correlation with behavior 1 week later showing that the among-individual correlation in behavior becomes more predictive of later behavior, later in life. Notice that the y-axis starts above zero. Source Data are provided as a Source Data file.