Tiny foxes on the Channel Islands lack not only mass, but also genetic variation and fear of humans

On the Channel Islands, 12-70 miles (20-113 km) off the Pacific coast of southern California, live six subspecies of the Channel Island Fox (Urocyon littoralis), a dwarf species that is a close relative of the gray fox living on the mainland (U. cineroargenteus). Genetic data suggest that these foxes have been isolated from the mainland species for about 9000 years, possibly brought to the islands by Native Americans who may have considered them sacred “spirit animals.”

Four of these subspecies are officially endangered, as their population sizes are fairly low—probably due to attacks by golden eagles and infection with canine distemper. They’re all holding on, though, and conservation efforts are increasing the population size. For now we don’t have to worry much about them.

These are adorable little animals, fully worthy of being Honorary Cats™. In contrast to the mainland species, whose individuals weigh between 8 and 15 pounds, these foxes have become dwarfed, weighing, according to a New York Times article by Carl Zimmer, as little as 2.3 pounds. For comparison, an average, non-obese house cat weighs between 6 and 10 pounds, so these foxes weigh about a third as much as a normal cat (or a fifth as much as Hili)! Subfossils show that the foxes were fully dwarfed by 7000 years ago, so it took only about two millennia for the small size to evolve.

Here’s a photo:

Credit: Chien Lee/Minden Pictures

Many animals that invade islands become dwarfed (“island dwarfism“), and for reasons we don’t fully understand. I suspect it has something to do with a dearth of food: if you’re big, you’re going to require lots of food to survive and reproduce, and may do better if you have genes for small size. But there are other explanations (see the link). Another example of the phenomenon are the famous dwarf elephants—shorter than a human—that lived on islands in the Mediterranean during the Pleistocene. (Curiously, the Channel Islands also harbored dwarf mammoths.)

And here’s a video showing their size and the adorableness of one subspecies, along with a description of how biologists are trying to save it. Do watch it, as it’s a good summary of the subspecies’ situation.

I’m bringing up this species because it’s the subject of a new paper by Jacqueline Robinson et al. in Current Biology (reference and link below, I don’t think there’s a free download). The paper shows that all six subspecies lack genetic variation; in fact, one of them is the vertebrate having the smallest amount of genetic variation ever observed. This finding belies the common conservationist notion that low genetic variation is always a warning that a species is endangered. And that notion itself comes from evolutionary theory: without genetic variation, you can’t respond to selective pressures such as new diseases, environmental changes, and so on; and if those pressures sufficiently reduce mortality or reproduction, a species with very low genetic variation might go extinct.

Here are the islands sampled:

The researchers did full-genome sequencing of every animal (something we only dreamed about two decades ago), and did it on one fox from each island, except for two foxes from San Nicolas Island as well as one mainland gray fox. Here’s the phylogeny of the foxes taken from that molecular data. The two foxes from San Nicolas were almost genetically identical, which I’ll discuss below. One thing this phylogeny shows is that the Channel Island fox subspecies are all more closely related to each other than to the Gray Fox putative ancestor. What that means (unless there was gene flow between island fox populations) is that all the island foxes descend from a single ancestor that got to one island, and then spread to the other island. If each island was colonized independently by a gray fox migrant, you wouldn’t get a phylogeny that looked like this:

The remarkable finding of this study was the extremely low genetic variation in all these subspecies, particularly in the San Nicolas subspecies, which had the lowest genetic diversity observed in any outbreeding (sexually reproducing) species. The authors call this phenomenon “genomic flatlining”, part of the paper’s title.

How, you might ask, can you estimate the genetic diversity of an entire subspecies if only a single individual was sampled? We can estimate this because we can look at both copies of a gene in a whole-genome sequence, and if they’re identical in DNA sequence, that implies that the entire species is depauperate in genetic variation. After all, each individual has two copies of each gene—getting one copy from its father and one from its mother. If both copies are the same, that implies that the population as a whole is pretty much genetically depauperate, with every individual having the same DNA sequence.

The different subspecies, however, were genetically different from each other, as expected given their morphological and color differences.

The San Nicolas fox had an amazingly low diversity, with the two individuals not only being homozygous at most DNA sites, but the two individuals were, as expected, nearly genetically identical to each other. They were the equivalent of identical twins, or clones, as the whole population must be. The heterozygosity of this population (calculated as π, or nucleotide diversity) was about 0.000016, with, on average about only 1.6 DNA sites in 100,000 showing a difference between maternal and paternal genes.

Here’s a figure showing the nucleotide diversity of various outbreeding species, with asterisks next to the fox subspecies. Letters show other species, including some, like the cheetah, once suspected to be endangered because of low genetic diversity. Note that the X axis (nucleotide diversity) is on a log scale, and the bars represent 159 outbreeding species in total. The foxes are way low, with the San Nicolas subspecies off the scale. For humans the value of pi is about 0.001, not far from the Santa Catalina fox, and for the fruit fly Drosophila π is about 0.01.

Caption from paper: C) Histogram showing the distribution of published genome-wide estimates of p from 159 outbreeding species (137 animal, 11 plant, 8 fungus, and 3 protist taxa; see the Supplemental Experimental Procedures), with the position of island and gray fox heterozygosity values indicated by asterisks. See also Data S1.

The other finding from this survey is that the fox populations, with San Nicolas again in the extreme, have high numbers of DNA sites where the effect on the individual is putatively bad: these include sites where any new substitution will affect the protein sequence (usually for the worse), and loss-of-function genes, for which the island populations simply don’t produce a protein where they should. There’s no direct evidence, though, that any of these changes are deleterious to survival and reproduction.

All island populations showed elevated levels of putatively deleterious genes in the genome. Population-genetic theory shows that small population sizes can, though the phenomenon of genetic drift (random changes in allele frequencies due to sampling effects), increase the frequency of genes that are bad. The rule of thumb is that if the population size is lower than the reciprocal of the selection against an allele, the allele will act as if it had no effect on fitness at all, and could reach high frequency by genetic drift. For example, a gene producing a reproductive deficit of 1% (0.01) compared to its alternative would be effectively neutral in populations smaller than 100 (1/0.01). And drift was certainly a possibility in this species, since the level of heterozygosity, as well as direct observation in recent years, suggested that some fox populations were once down to about 10-100 individuals.

The upshot: Despite low population size, these fox subspecies are doing well, although conservationists warn us that such low levels of genetic variation can be harmful and promote extinction. It may be that the conservation efforts, combined with an environment that is fairly benign, ameliorate the effects of low genetic variation.

And did I mention that these foxes are tame? As Carl Zimmer noted in his piece:

“They’re like dodos,” Dr. Wayne [director of the study] said in an interview. “They have no notion of human fear. You can just put them in your lap.”

I’d love to do that!

_________

Robinson, Jacqueline A., D. Ortega-Del Vecchyo, Z. Fan, Bernard Y. Kim, Bridgett M. vonHoldt, Clare D. Marsden, Kirk E. Lohmueller, and Robert K. Wayne. Genomic Flatlining in the Endangered Island Fox. Current Biology, in press. doi:10.1016/j.cub.2016.02.062