Molecular Natural History is a series of posts highlighting what population genetic data has revealed about some of my favorite organisms. There’s no rhyme or reason to what species I’ll feature for this, beyond the fact that they’ve made me stop and look closer when I see them along a trail or in my neighborhood, and I need to find at least a little interesting research addressing their molecular ecology.
California’s Channel Islands, an archipelago tucked into the bight formed by concave coastline between Conception and San Diego, are home to a long list of endemic flora and fauna. Of these, the Channel Island foxes, Urocyon littoralis, are arguably the most charismatic — and unquestionably the cutest. They are sister species of the gray fox, and have very similar coloration, but they’re as little as half the size, or a third of the mass, of their mainland congener. It’s not unusual for animals to evolve dramatically smaller (or greater) body size on isolated islands, and the Channel Island foxes provide a case study of the phenomenon within an hour’s boat-ride from Los Angeles.
I’ve been to two of the Channel Islands in a half-dozen years living in Southern California, but I’ve only seen Channel Island foxes on Santa Cruz, the largest of the islands protected in Channel Islands National Park. The Santa Cruz foxes have very little fear of humans, and despite being smaller than house cats, they are the largest terrestrial predator on the island. A dozen or so of them have the run of the National Park campground at the eastern end of the island, and spending two nights there was, truly, like camping in a cat café.
During the day, tiny foxes were on constant patrol for unguarded snacks. The Park staff and visitor information are very clear about the penalties for feeding wildlife — and about the foxes’ ability and willingness to nose open unlocked coolers and even un-zip tent flaps. We lost count of the times we saw foxes hop up on picnic tables or inspect backpacks on the ground within a few yards of temporarily distracted campers. Or they would simply nap. One curled up in the unoccupied tent site next to ours for most of an afternoon.
It’s possible the foxes came by their comfort with humans before they shrank. Native peoples first settled on the Channel Islands at least 13,000 years ago, and the earliest archaeological evidence of island foxes is substantially more recent. Radio-isotope dating of fox remains, and the archaeological evidence that many of those remains were found in close association with human habitation, indicate that Native people brought the foxes from the Northern Channel Islands to the southern Channel Islands about 5,000 years ago — maybe for their fur, maybe because to control rodent populations, or maybe, simply, as pets.
The southern islands are too far from the mainland for foxes to have arrived there on their own; the northern ones are closer, and have been even more accessible in the past, when sea levels were lower during the last ice age. But the earliest archaeological and paleontological record of foxes on the northern islands only dates to about 7,000 years ago. In that time-frame, they might have “rafted” from the mainland on floating plant debris, but they may very well have been brought by people who had already established communities on the islands. This is the first point at which genetic data helps us unravel the island foxes’ history: A 2016 study of mitochondrial genomes found differences between Channel Island foxes and mainland gray foxes consistent with a split from a common ancestor about 9,200 years ago.
That mitochondrial data also found that the island foxes carried substantially less diversity in their DNA sequences, and had acquired more non-synonymous substitutions, than mainland gray foxes. These are the expected results of population bottlenecks like founder events — island populations established by just a few individuals. Subsequent analysis based on sequence data from thousands of loci in the nuclear genome supports this model, finding that divergence from mainland gray foxes is associated with reduced genetic diversity in the island foxes. This is as expected if genetic drift is most responsible for differences among foxes on separate islands.
The island foxes have also faced a much more recent bottleneck, in the form of a brush with extinction in the 1990s. They were the victims of a veritable ecological domino-run: bald eagles, long the biggest predator on the islands, declined due to the effects of DDT, and golden eagles established breeding sites in their wake. Bald eagles mostly eat fish, but golden eagles like more terrestrial prey, such as feral pigs that had been introduced earlier in the 20th Century — and also tiny foxes. They hunted the foxes down to populations as small as fifteen individuals on some of the islands, and the foxes only rebounded thanks to dedicated efforts to remove golden eagles and re-establish resident bald eagles.
Recovery from such a sharp bottleneck may be limited by the loss of genetic diversity in the bottleneck — a small population with little diversity has less capacity to adapt to environmental change, and may suffer “inbreeding depression,” accumulating deleterious recessive genetic variants. More intensive genetic data collection suggests, however, that the island populations have been small and homogenous since at least the early 20th Century, and seem to be doing all right despite this. A 2018 study compared whole-genome sequence data from mainland foxes to island foxes sampled recently and as early as 1929, and found that the recent samples were not necessarily less diverse than the early ones.
The authors of that study also found more potentially deleterious variation in the genome sequences of island foxes compared to their mainland cousins — but they examined skeletons of island foxes and found they had substantially fewer developmental anomalies than seen in populations of other canid species with known histories of inbreeding depression. They simulated evolution under a number of scenarios paralleling the possible origins of the island fox populations, and found that, in fact, natural selection removed moderately and strongly deleterious recessive mutations from the island population more efficiently than it did from the larger mainland population.
Small population size and low genetic diversity might be a concern for the Channel Island foxes in the longer term, as they accumulate more weakly deleterious variants — but for now they seem to be holding up just fine. Their island homes are hardly extensive, which creates some inevitable precarity, especially as climate change reshapes habitats everywhere. However, most of those islands also enjoy a high degree of protection, and it’s hard to come up with a species of conservation concern with more charisma than fearless, miniaturized foxes. I’m hopeful they’ll be burgling campers’ lunches for a long time to come.
References
Benítez-López A., L Santini, J Gallego-Zamorano, B Milá, P Walkden, MA Huijbregts, and JA Tobias. 2021. The island rule explains consistent patterns of body size evolution in terrestrial vertebrates. Nature Ecology & Evolution, 5(6), 768-786. doi.org/10.1038/s41559-021-01426-y
Funk WC, RE Lovich, PA Hohenlohe, CA Hofman, SA Morrison, TS Sillett, CK Ghalambor, JE Maldonado, TC Rick, MD Day, NR Polato, SW Fitzpatrick, TJ Coonan, KR Crooks, A Dillon, DK Garcelon, JL King, CA Boser, N Gould, and WF Andelt. 2016. Adaptive divergence despite strong genetic drift: genomic analysis of the evolutionary mechanisms causing genetic differentiation in the island fox (Urocyon littoralis). Molecular Ecology 25(10): 2176-2194. doi.org/10.1111/mec.13605
Hofman CA, TC Rick, MTR Hawkins, WC Funk, K Ralls, CL Boser, PW Collins, T Coonan, JL King, SA Morrison, SD Newsome, TS Sillet, RC Fleischer, and JE Maldonado. 2015. Mitochondrial Genomes Suggest Rapid Evolution of Dwarf California Channel Islands Foxes (Urocyon littoralis). PLOS ONE 10(2): e0118240. doi.org/10.1371/journal.pone.0118240
Rick TC, JM Erlandson, RL Vellanoweth, TJ Braje, PW Collins, DA Guthrie, and TW Stafford, Jr. 2009. Origins and antiquity of the island fox (Urocyon littoralis) on California’s Channel Islands. Quaternary Research 71:93-98. doi.org/10.1016/j.yqres.2008.12.003
Robinson JA, C Brown, BY Kim, KH Lohmueller, and RK Wayne. 2018. Purging of strongly deleterious mutations explains long-term persistence and absence of inbreeding depression in island foxes. Current Biology 28(21):3487-3494. doi.org/10.1016/j.cub.2018.08.066
Sacks BN, MJ Statham, LEK Serieys, and SPD Riley. 2022. Population genetics of California gray foxes clarify origins of the island fox. genes 13:1859. doi.org/10.3390/genes131001859
