Lifetime development of behavioural phenotype in the house mouse (Mus musculus)

Abstract

With each trajectory taken during the ontogeny of an individual, the number of optional behavioural phenotypes that can be expressed across its life span is reduced. The initial range of phenotypic plasticity is largely determined by the genetic material/composition of the gametes whereas interacting with the given environment shapes individuals to adapt to/cope with specific demands. In mammalian species, the phenotype is shaped as the foetus grows, depending on the environment in the uterus, which in turn depends on the outer environment the mother experiences during pregnancy. After birth, a complex interaction between innate constitution and environmental conditions shapes individual lifetime trajectories, bringing about a wide range of diversity among individual subjects. In laboratory mice inbreeding has been systematically induced in order to reduce the genetic variability between experimental subjects. In addition, within most laboratories conducting behavioural phenotyping with mice, breeding and housing conditions are highly standardised. Despite such standardisation efforts a considerable amount of variability persists in the behaviour of mice. There is good evidence that phenotypic variation is not merely random but might involve individual specific behavioural patterns consistent over time. In order to understand the mechanisms and the possible adaptive value of the maintenance of individuality we review the emergence of behavioural phenotypes over the course of the life of (laboratory) mice. We present a literature review summarizing developmental stages of behavioural development of mice along with three illustrative case studies. We conclude that the accumulation of environmental differences and experiences lead to a "mouse individuality" that becomes increasingly stable over the lifetime.

Keywords: adolescence; adulthood; behavioural phenotype; behavioural stability; life stages; ontogeny; phenotypic plasticity; post-reproductive age; postnatal; prenatal.

Figure 1

Development of physiology and behaviour over the lifetime of a mouse. Events are indicated at the mean time point of their occurrence according to the literature record including various non-genetically modified strains of mice. Detailed information on the expression of single traits can be found in the corresponding text sections.

Figure 2

Enhanced spatial memory in offspring of mothers with physical activity during pregnancy. Transgenic (tg) and wild type (wt) mice modelling Alzheimer's disease were tested for spatial memory in a Barnes maze. The mothers of half of the animals were physically active by using a running wheel (RW) during pregnancy while the other mothers lived in standard housing (SH) conditions without access to a running wheel. None of the mice tested as adults at an age of 136 days had access to a running wheel themselves. Offspring of running mothers performed significantly better in the test, indicating a long lasting effect of environmental conditions during pregnancy on cognitive behaviour in adult offspring. Figure redrawn after [103].

Figure 3

Repeatability of activity measures increases with age. 40 female mice (strain C57BL/6) were housed in a semi naturalistic environment and automatically tracked using RFID transponders and 20 Ring antennas [103,104]. Activity was measured from PND 35 (mid adolescence) to PND 125 (adulthood) by total antenna contacts measured in bouts of 5 days. The figure shows the repeatabilites taken from generalised linear mixed models (GLMM) including age at testing as a fixed and animal ID as a random factor. Each repeatability measure is calculated over three adjacent measurements of activity. The grouping of data is indicated on the x-axis. In green, the 95% confidence intervals of the repeatabilities are given. With the exception of the very first repeatability measurement taken between day 35 and 45, all repeatabilities are significant. As a general trend, the older the animals grew, the better the predictability for their future activity got.

Figure 4

Persistent individual differences despite standardisation. 40 female mice of the inbred strain C57BL/6 were kept in strictly standardised conditions and tested at PND 85 and PND 120 in an open field (OF) test for locomotor behaviour. Despite genetic and environmental standardisation considerable individual differences emerged in both tests. Pearson's product-moment correlation analysis revealed a significant correlation between the different tests explaining 13% of the variance. Additionally to the regression line (black) the 95% confidence band (inner red lines) and the 95% prediction band (outer blue lines) are drawn.