Turns out, bigger isn’t always better: Why snow voles haven’t evolved to be giants

Bigger animals are typically more fit, and body size is heritable, so one would expect to see body size increase in populations across generations. However, countless studies of wild animal populations haven’t shown this to be the case. Recent research publishing on January 26th, 2017 in the open access journal PLOS Biology provides new evidence and theory to explain why. This new work, from Timothée Bonnet, University Zurich, Switzerland, and colleagues, which studies a population of alpine snow voles, reveals new insights into why body size is maintained.

An animal has higher fitness if it is more likely to reproduce and pass its genes on to the next generation, and fitness is influenced by both genes and the environment. By analyzing nearly a decade’s worth of data on the morphology and fitness of snow voles, the authors confirmed that heavier individuals indeed had higher survival and reproduction rates.

The authors investigated how body mass and relative fitness varied at the level of both the genes (the “genotype”) and the physical traits (the “phenotype”). At the phenotypic level they saw the expected positive correlation between mass and fitness, but unexpectedly and counterintuitively, the found that at the genetic level there was no corresponding positive correlation — instead they found evidence for genetic change towards smaller, not larger, size.

The authors ruled out several possible explanations for why there might be a genetic change towards smaller size, including some sort of trade-off between increased body size and reduced fitness through correlated changes, but they found no evidence for other morphological traits or changes in fecundity that might provide opposing selection on size. They next investigated if they were failing to account for a critical phenotypic trait in their analysis — known as a “missing” trait. This work revealed that there were two “missing” traits in their analyses.

The first “missing” trait is the exact age at which the juvenile was caught and weighed in its first summer; this could not be directly measured and thus wasn’t included in the analyses. The second is the length of time it takes for an individual to achieve its adult body mass. For bsnow voles, it’s important that the new-born pups reach their adult size before winter; individuals that take longer to develop face a high risk of mortality if snowfall is early, as it has been in recent years. This selection for shorter development times leads to a selection for smaller body mass.

There are two key conclusions of this work. First, the apparent positive selection for increased body mass is confounded by sampling populations at different ages. Second, “phenotypic selection for larger size” is not causal, that is, it does not represent an effect of mass on fitness, but is mediated by age and environment quality, and therefore it cannot lead to genetic change. Phenotypic selection for shorter development time is causal and therefore can be observed at the level of gene and lead to genetic change. Whether these conclusions hold for other wild animal populations will need to be tested. Lastly, this study shows how climate change might affect wild populations in more ways than just rising temperatures and timing of reproduction in the spring; Changes in the annual cycles of weather, including timing of first snowfall, can have profound effects on wild animals.


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Citation: Bonnet T, Wandeler P, Camenisch G, Postma E (2017) Bigger Is Fitter? Quantitative Genetic Decomposition of Selection Reveals an Adaptive Evolutionary Decline of Body Mass in a Wild Rodent Population. PLoS Biol 15(1): e1002592. doi:10.1371/journal.pbio.1002592

Funding: The study was funded by a Swiss National Science Foundation ( project grant (31003A_141110) awarded to EP. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing Interests: The authors have declared that no competing interests exist.