Climate change ecology: Hot under the collar

A 34-year study of collared flycatchers demonstrates that males are evolving to be less ornamented in response to rising temperatures.

For male collared flycatchers (Ficedula albicollis; pictured), having a large white patch on your forehead signals that you are a fearsome rival, and an attractive mate. But while large patch size was thought to give males an evolutionary advantage, it seems that climate change is turning this advantage on its head. In this issue of Nature Ecology & Evolution, Evans and Gustafsson1 report that the collared flycatcher's forehead patch has declined in size because large patch males have lower fitness as the climate warms.

In many animals, males have ornamental features that are used to attract mates, and to signal to rivals during territorial interactions. While these ‘sexually selected’ ornaments can increase a male's mating success, they can also impose a variety of costs on their bearers. Ornaments such as bright colouration can increase susceptibility to predators, or they can predispose males to competing for larger territories and more mates, at the expense of providing care for their offspring. As a result, ornamental traits are hypothesized to evolve only when the benefits of being ornamented outweigh the costs2.

Since many of the costs of being ornamented could change with changing environmental conditions, some researchers have speculated that climate change could have widespread effects on animal ornamentation. In some previous studies, changes in ornamentation have been observed that seem to be linked to climatic conditions3,4. However, whether these changes are due to individual flexibility in ornament expression, or whether ornaments are evolving in response to consistent environmental change, is not clear

Using a long-term study of collared flycatchers on the Baltic island of Gotland, Evans and Gustafsson tracked changes in forehead patch size. The researchers noted that males had become less ornamented over time, with mean forehead patch size decreasing about 10% between 1981 and 2014. Because collared flycatchers breed in the same site each year, and return to the site where they were hatched, the authors knew the identity of each individual's mother and father. Using this information, they could then distinguish whether changes in forehead patch size were due to changes in the underlying genetics, or whether they were simply a flexible response to changing environmental conditions. The authors found that there had indeed been genetic changes related to forehead patch size, demonstrating a true evolutionary change in ornamentation.

Credit: JOHAN TRÄFF

Historically, male collared flycatchers with larger forehead patches were at an advantage because they could secure better territories and raise more offspring5. Consistent with this expectation, the authors found that males with large forehead patches had higher fitness than males with small patches in the early years of the study. However, this pattern reversed sometime between 1995 and 2000. In seven of the eight most recent years, males with small forehead patches had higher fitness than those with large patches, demonstrating, incredibly, a complete reversal in selection over the study period.

Importantly, the authors noted that the strength of selection on forehead patch size was correlated with local climate conditions. Following warmer springs, small-patched males performed relatively better than during years following colder springs. Since the average spring temperature increased by 1.5 °C over the study period, this ultimately tipped the scales in favour of small-patched males in this population. Interestingly, the component of fitness that was most influenced by climate was survival. Large-patched males were less likely to survive as climate warming progressed, suggesting that climate change was increasing the costs of ornamentation in this species.

While the authors demonstrate a strong link between climate warming and selection on male ornamentation, they were not able to determine the mechanism behind this link. Predicting the effects of climate change on ornamentation will be challenging because environmental and ecological changes have complex interactions with the dynamics of sexual selection6. However, the most dramatic effects of climate change will probably be caused by changes in biotic interactions7. For example, climate change can lead to the introduction or removal of predators, parasites and competitors7, and these altered biotic interactions could have a strong impact on the costs of ornamentation. Indeed, the authors suggest that local decreases in the density of pied flycatchers (F. hypoleuca) could have something to do with the decline in forehead patch size in collared flycatchers. Pied flycatchers also have a white forehead patch, and collared flycatchers are known to evolve larger forehead patches when the two species co-occur, in an effort to avoid hybridization8.

Certainly, there are good theoretical reasons why climatic changes could influence animal ornamentation across the globe. As Evans and Gustafsson show, some ornaments will decline in response to environmental change, and it is conceivable that some ornaments could disappear altogether2. However, there are also reasons to predict that climate change will drive the evolution of new, or exaggerated, ornaments in some species6. Just as climate change will lead to winners and losers in terms of species’ abundance and distribution, it seems it may also lead to winners and losers in the global beauty pageant.

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Correspondence to Cody J. Dey or James Dale.

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Dey, C., Dale, J. Climate change ecology: Hot under the collar. Nat Ecol Evol 1, 0060 (2017). https://doi.org/10.1038/s41559-016-0060

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