Data on three generations of Antarctic fur seals suggest that climate change is reducing the survival of less-fit individuals with low genetic variation, but that overall seal numbers are falling. See Letter p.462
A little more than a century ago, humans had pushed Antarctic fur seals (Arctocephalus gazella) to the brink of extinction. Once hunting stopped, their numbers rose, and by the early twenty-first century their population had grown to a few million. On page 462 of this issue, Forcada and Hoffman1 show that breeding fur seals on the beaches of South Georgia Island in the southern Atlantic are, on average, becoming more heterozygous — an indicator of individual genetic variability that is linked to improved survival and reproductive success. At face value, this seems to be good news, but a more detailed look reveals that it is a worrying symptom of a population that is again declining.
Offspring of sexually reproducing organisms receive one strand of DNA from their mother and another from their father. Some points along the two strands are the same and others are different; the more differences, the more heterozygous an individual is said to be. Higher heterozygosity frequently correlates with an individual's ability to successfully survive and reproduce — more-heterozygous individuals are fitter2,3,4.
Using individual-level data on the survival, reproduction and genetics of multiple generations of fur seals coupled with data on stocks of krill (the seals' main food) and weather conditions in the southern oceans, Forcada and Hoffman tested whether there have been changes in the size of the population and the heterozygosity of the fur seals that are associated with changing environmental conditions. They found that there has been no change in the heterozygosity of seal pups born, but that there has been an increase in the mortality rates of less-heterozygous individuals compared with those of higher heterozygosity. This means that only the more-heterozygous individuals are surviving to breeding age. But the data also show that these individuals begin breeding later in life, and breed less frequently. During the course of the study, the authors report a decline in population size of nearly 25%, and a per-generation increase in the heterozygosity of breeding females of 8.5%.
The reason that these breeding animals are not producing more-heterozygous offspring is that heterozygosity is a complex function of how different each parent is at each point along the strands of DNA they pass to their offspring. Two highly heterozygous parents may be just as likely to produce an offspring with low heterozygosity as they are to produce one that is highly heterozygous. Heterozygosity itself is not heritable and, consequently, the population cannot adapt to change through evolving levels of heterozygosity (Fig. 1). But why are we seeing elevated mortality rates in the less-heterozygotic individuals?
To investigate this, Forcada and Hoffman constructed a simulation model of the number of breeding females, incorporating a measure of climatic variation in the southern oceans and observed variation in the availability of krill. The model provided predictions that matched well with observed fluctuations in population size, suggesting that recent declines in fur-seal numbers have been driven to a large extent by changes in weather patterns that have reduced the availability of krill. Other factors may have also affected krill availability, including changes in fishing practices5 and increased whale numbers6.
The authors found that a model including krill availability and climatic variation predicted observed population sizes a little better than one that included only climatic variation, which suggests that increases in fishing pressure and whale numbers may have also contributed to the recent decline in the fur-seal population. These changes have had a disproportionately greater effect on fur seals with low heterozygosity than those with higher values, leading to a simultaneous decline in population size and an increase in the heterozygosity of breeding females (Fig. 1).
Why does any of this matter? One of the biggest unknowns in predicting how our planet's weather will continue to change in the future — arguably the biggest threat that humanity faces over the coming century — is how animals, plants and the ecosystems they form will respond to changing carbon dioxide levels, and how these changes will feed back to influence the global climate. We have few studies that adequately explore the response of natural systems to environmental change, because collecting the necessary data is challenging and simple surveys of one or two aspects of a population or ecosystem are often insufficient to provide useful understanding. If Forcada and Hoffman had solely focused on the trend in heterozygosity among seals, they might have concluded that the future for the seals is bright because they are getting fitter. But the detailed, long-term, individual-based data reveal a completely different, and altogether less rosy, picture.
Fortunately, technological advances now mean that ecologists and ecosystems scientists can gather considerably more data that are appropriate for assessing how the natural world is responding to climate change, and how these responses feed back to either decrease or accelerate rates of change. Such technology is not cheap, and investment from government and industry is required for its deployment. But once that happens, we will be able to get a much clearer picture as to whether the fur seals of South Georgia are unusual in their response to anthropogenic change, or whether such genetic and ecological dynamics are typical. Either way, it may be much harder to arrest the ongoing decline in fur seals in the twenty-first century than it was in the twentieth.