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:

26ZIMMER-master768

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:

Screen Shot 2016-04-28 at 7.45.02 AM

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:

Screen Shot 2016-04-28 at 7.45.18 AM

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.

Screen Shot 2016-04-28 at 7.45.29 AM

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

63 Comments

  1. Cindy
    Posted April 28, 2016 at 9:20 am | Permalink

    They remind me of my tiny Abyssinian kitty.

    PCC, you left out the House Hippo, as documented in this fine Canadian PSA (House Hippos are native to Canada)
    http://www.theloop.ca/they-lied-the-tiny-house-hippo-is-very-real-and-we-have-proof/ (watch the second video)

    • Diana MacPherson
      Posted April 28, 2016 at 9:28 am | Permalink

      I love the House Hippo!

  2. Posted April 28, 2016 at 9:27 am | Permalink

    This is an excellent overview, thank you Jerry.

  3. Diana MacPherson
    Posted April 28, 2016 at 9:28 am | Permalink

    I want to kiss those cute foxes!

  4. Posted April 28, 2016 at 9:31 am | Permalink

    “‘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.'”

    This morning I’m dreaming about hiking around that island and taking a nap, supposing there’s no poison ivy (otherwise all over the CA coast). If one of these sweet, gorgeous pups crawled up on my stomach, I would not object.

    Thanks for writing about this.

    • Posted April 28, 2016 at 9:32 am | Permalink

      I meant poison oak (not ivy).

    • Diana MacPherson
      Posted April 28, 2016 at 9:58 am | Permalink

      I often dream of taking naps.

      • Posted April 28, 2016 at 11:36 am | Permalink

        I want one right now. Crawl under my desk. Cover myself with blanket and doze for 30 minutes. I absolutely will at some point today. But right now, I need to look something up on the UCSC Genome Browser before I forget. You know waking up from a nap can be disorienting? Better do the search while my head is working.

        • Diana MacPherson
          Posted April 28, 2016 at 5:41 pm | Permalink

          Yes, I often discuss, with my colleagues, about how George Costanza was right and that my desk could totally work as a bed underneath it.

  5. Erik
    Posted April 28, 2016 at 9:33 am | Permalink

    The timing of the story and this post are ideal for me. We had just finished covering Inbreeding, Inbreeding depression, and this case in my (non-majors) Honors Biology class. If they were Biology majors, I’d have them read the primary research paper, but this post is an excellent follow-up to what we discussed in class. Another aspect of the Channel Island foxes is the apparently successful program to relocate Golden Eagles that were predators on the foxes and disrupted the food webs of the islands: http://www.pnas.org/content/99/2/791.full

    • Purshia
      Posted April 28, 2016 at 9:55 am | Permalink

      I’m in a similar position, Erik. We just finished our unit on evolution and natural selection (the exam is this morning) and we’re moving on to species interactions next week. I’ll have to be satisfied with giving my students a link to this post and urging them to pursue this on their own. My class is a non-science majors course. I’m quite pleased, though, with how much genuine interest most the students have in learning about evolution.

    • HBB
      Posted April 28, 2016 at 4:29 pm | Permalink

      Same here, almost. I just finished talking about island gigantism and dwarfism in my biogeography class (for biology majors). As noted down-thread – Oh, the probability . . .

  6. Posted April 28, 2016 at 9:51 am | Permalink

    Populations that recently reached low sizes tend to bring with them some of the harmful alleles present in big populations, and so tend to face problems, e.g. Florida Panthers and their male sterility.

    However, I’ve read that populations that remain small for prolonged periods of time, e.g. 9000 years, either loose (“purge”) their harmful alleles or didn’t have them at the start (for otherwise they wouldn’t survive that long). The point of the article I remember best is that very small population sizes aren’t necessarily genetically doomed, so they’re worth protecting.

    You write above that somewhat harmful alleles are effectively neutral in these small populations. Is the apparent discordance between these concepts a function of selection pressure, so mildly deleterious alleles may be kept, or is the idea reported in my second paragraph untrue?

  7. Michael Finfer, MD
    Posted April 28, 2016 at 9:55 am | Permalink

    Doesn’t a lack of genetic diversity, while not necessarily a sign of impending extinction, put a species at risk of some undefined catastrophe?

    I am thinking in particular of the Tasmanian Devil, which was hunted nearly to extinction a century or a century and a half ago, and now is suffering from a transmissible cancer, presumably because each individual is so similar to the others that their immune systems cannot recognize the cancer as foreign.

    I assume that an introduced infection of some sort could have a similar effect.

    If my thinking has gone astray, I would appreciate it if someone sets me straight.

    • JohnW
      Posted April 28, 2016 at 10:23 am | Permalink

      HA! I was thinking the very same thing…at the very same time. Oh, the probability…

    • Posted April 28, 2016 at 11:29 am | Permalink

      I think you are thinking quite straight.

  8. Peter M
    Posted April 28, 2016 at 10:04 am | Permalink

    In the article you said the following “If both copies are the same, then that implies that the population as a whole is pretty much genetically depauperate, with all individuals having the same DNA sequences.”

    I am not a biologist, but I was wondering about the following question: do they also take into account that the selected Fox could be the result of e.g. sister/brother inbreeding and that the pick was just unlucky?

    • Posted April 28, 2016 at 10:08 am | Permalink

      Yes, that’s a good question, and I considered writing about it but decided it was a bit arcane. It is possible that such homozygosity could be cause by inbreeding of rare individuals, but both Channel Island foxes (blood collected a long time ago) were not only homozygous, but identical. Unless those foxes were the result of persistent, long-term inbreeding, the greater likelihood is that the homozygosity and identity (and the homozygosity of other island foxes) is due to genetic drift rather than, say, brother sister mating.

      Complicating this issue is that, in principle, genetic drift is the same thing as inbreeding, but we won’t get into that. . .

  9. rickflick
    Posted April 28, 2016 at 10:09 am | Permalink

    sub

  10. JohnW
    Posted April 28, 2016 at 10:11 am | Permalink

    Thanks I’ll have to check out the paper.

    Wondering if while effectively neutral due to small population size, this population’s load of deleterious alleles might actually provide a constraint on overpopulation by increasing infant mortality?

    Also, while they have persisted for a somewhat astonishingly long time, they do appear to be living on the edge when one considers what’s happening to the Tasmanian devil.

  11. Posted April 28, 2016 at 10:17 am | Permalink

    Would it be worthwhile to swap a few foxes between islands to increase the genetic diversity?

    • Posted April 28, 2016 at 10:59 am | Permalink

      They’ve suggested that, but of course that effaces the subspecies, and the idea has been rejected.

    • gravelinspector-Aidan
      Posted April 28, 2016 at 5:19 pm | Permalink

      There was a somewhat similar case reported a few years ago of an isolated wolf pack in Southern Sweden that was suffering from inbreeding, reduced reproductive success, etc for years. Then in the mid-1990s a single wolf made it across the isolating barrier from N.Sweden and the subsequent injection of diversity greatly improved the success of the pack as a whole.
      Mixing populations is certainly doable, but they’re seemingly keeping that trick in reserve for if thing get desperate.

  12. Mark Sturtevant
    Posted April 28, 2016 at 10:34 am | Permalink

    I teach about the island foxes in my evolution class. There, the story I tell is how species introduction has consequences on other species, and that it can be complex. I got this from the textbook that I use. The scenario is:
    a) Pigs were introduced to the islands.
    b) This attracted the golden eagles which hunt the pigs, but also…
    c) they are now hunting the foxes more often then they used to. Because the foxes are in decline…
    d) there is an increase in the # of spotted skunks which were hunted by the foxes.

    • Posted April 28, 2016 at 10:43 am | Permalink

      “Golden eagles, feral pigs, and insular carnivores: How exotic species turn native predators into prey”

    • Beau Quilter
      Posted April 28, 2016 at 11:27 am | Permalink

      I wonder if the eagle predation might drive an evolutionary shift towards larger foxes.

    • rickflick
      Posted April 28, 2016 at 1:25 pm | Permalink

      “c) they are now hunting the foxes more often then they used to. Because the foxes are in decline…”

      Shouldn’t it be “Because the pigs are in decline…” ?

      • Mark Sturtevant
        Posted April 28, 2016 at 4:04 pm | Permalink

        Yes, that is a better way to put it. What I was getting at was that the foxes are in decline due to hunting by eagles.

        I did not know of the added (and more serious problem) of canine distemper that was introduced to the islands. This is another teachable detail. What this section of the course is about is on the various causes of extinctions of species. Two of the factors I bring up are introduced species which upset the balance, and introduction of diseases. So both are going on here.

  13. Beau Quilter
    Posted April 28, 2016 at 11:26 am | Permalink

    Jerry mentioned a dearth of food as driver of their evolutionary dwarfism. I was thinking of two other factors that might play a role: the size of their available prey on the islands, and the dearth of fox predators for which larger size might be a deterrent.

  14. Posted April 28, 2016 at 11:32 am | Permalink

    Dwarf Mammoths. An oxymoron like giant shrimp.

    • frednotfaith2
      Posted April 28, 2016 at 12:07 pm | Permalink

      Actually, since mammoth and shrimp are the names of specific types of animals, the designations “dwarf” or “giant” of particular species of mammoth and shrimp are not oxymorons at all but are apt descriptions of a species of mammoth much smaller than other mammoths and shrimp species larger than most.

      • Posted April 28, 2016 at 12:13 pm | Permalink

        Yes, I know that. I didn’t have anything better to say and needed to show the science posts are being read.

    • gravelinspector-Aidan
      Posted April 28, 2016 at 5:29 pm | Permalink

      The very last mammoths on the planet (to date) were on th Wrangle I lands off extreme NE Siberia. They were up to 1.5m at the shoulder. Which is moderately amazing.
      They were contemporaries of Pyramid Builders and proto – Jewish-or-Muslim goat-herders in the Levant. And that I find totes amazeballs.

      • Jonathan Wallace
        Posted April 30, 2016 at 4:09 am | Permalink

        Yes, that’s a fact that always impresses me.

  15. TJR
    Posted April 28, 2016 at 11:37 am | Permalink

    Not what I was expecting when I saw “Channel Islands”, but very interesting stuff.

    Maybe the foxes are inbreeding as a tax dodge?

    • Richard
      Posted April 29, 2016 at 4:12 am | Permalink

      Me neither. 😦

      But the *real* Channel Islands don’t have such gorgeous foxes; or badgers, or otters, or squirrels, or (wild) deer, or stoats, or weasels, or …

  16. Merilee
    Posted April 28, 2016 at 11:40 am | Permalink

    Fascinating ( totes amazeballs)

  17. loren russell
    Posted April 28, 2016 at 11:57 am | Permalink

    “Brought as ‘spirit animals’ by Native Americans.”

    It may be question-begging to use concepts of [some] contemporary Native Americans for 9000 bp people.

    But deliberate introduction of foxes is certainly possible, and might have been done for fairly utilitarian purposes, or even as pets — assuming that in the absence of small felids, foxes were likely seen as useful mousers wherever Native people stored food.. Like old world kitties, they might be tolerated, then encouraged, perhaps even adopted as kits, played with by children.

    • Posted April 28, 2016 at 12:05 pm | Permalink

      Here’s what Zimmer said, which was the source of what I said:

      “It’s unlikely the foxes made the trip on their own; the islands are separated from the mainland by 12 to 70 miles of open ocean. Another clue pointing to human help: Native Americans painted foxes on rocks and gave them ceremonial burials. Foxes may have had a spiritual importance to them.”

      Note that you are misusing “question-begging” here: it means to assume what you want to prove.

      • loren russell
        Posted April 28, 2016 at 1:01 pm | Permalink

        I hesitated on the term, but I thought the rather theory-laden “spirit animal” is an example of forcing a religious reading into actions that might have many other contexts.

        So the question being begged here was whether religious concepts of people living 9000 years ago had much to do with recent ideas that have been popularized to connote a particular connection of native peoples to their environment. Note that at 9000 bp, the California natives had just mopped up the last of one of the great megafaunas. If they were thinking then in terms of spirit animals, it’s a shame they didn’t adopt and protect some ground sloth or pygmy mammoth..

        In any case, I rather like the picture of children smuggling their favorite fox kits in baskets on their families relo to the islands.

  18. Posted April 28, 2016 at 12:08 pm | Permalink

    I have no direct comment on the content, but I do find that list of animals on the histogram C fun. Yangtze dolphins and a species of mosquito on one graph! Nifty 😉

  19. Andrew Liffrig
    Posted April 28, 2016 at 1:02 pm | Permalink

    Did anyone compare the DNA of these Channel Island foxes to the Russian Domesticated Red Fox? I wonder if the lack of fear of humans is related to the same genes that got selected for in that breeding project, and if so, that any canine might be able to be domesticated in the same way wolves were.

  20. Denis Westphalen
    Posted April 28, 2016 at 1:26 pm | Permalink

    When I look at the phylogeny chart I wonder: where/when did the dwarfism take place? Several times at each the parallel branch or just once before the island foxes split from the gray fox?

    Also, what is the meaning of the numbers on the phylogeny chart?

    • jaxkayaker
      Posted April 28, 2016 at 4:13 pm | Permalink

      Those numbers are measures of genetic distance used in a tree building algorithm known as neighbor-joining. Each number is the amount of genetic differentiation accumulated in the lineage since the preceding node, or branch point. These can be totaled back to any node, which represents a most recent common ancestor population. Bootstrapping (see below) is a method of testing the strength of support for a particular tree (particular arrangement of branch points).

      Figure caption: Neighbor-joining tree constructed from a genome-wide pairwise distance matrix, displaying reciprocal monophyly of northern and southern island populations and the southern California gray fox as the outgroup. Genetic distance is indicated on the branches. All nodes have 100% bootstrap support.

      http://www.sciencedirect.com/science/article/pii/S0960982216301737

      Thanks for the post, Jerry. Let me know how good or bad my explanation was.

      • Denis Westphalen
        Posted April 28, 2016 at 4:50 pm | Permalink

        Thanks. I will check the link.

  21. JHeardJr
    Posted April 28, 2016 at 1:31 pm | Permalink

    Could Homo floresiensis, a now extinct small in stature hominid, found on an Indonesian island, also be the result of “island dwarfism”?

    • gravelinspector-Aidan
      Posted April 28, 2016 at 5:23 pm | Permalink

      That was certainly part of the discussion at the time.

      • Mike
        Posted April 29, 2016 at 8:11 am | Permalink

        There were also Dwarf Elephats extant at that time on the Island which the Hobbits are supposed to have Hunted.

        • gravelinspector-Aidan
          Posted April 29, 2016 at 10:14 am | Permalink

          Oh yes, I’d forgotten them.
          Dwarfed elephants all over the Mediterranean … the sub-fossil skulls have been proposed as sources for the myth of the Cyclops, with the one big nasal orifice being sufficiently eye-like … each one succumbing to the spears of human hunter-gatherers as they arrived. Awwww!

  22. Randy Schenck
    Posted April 28, 2016 at 2:05 pm | Permalink

    Really great posting. Lots to learn from the post and comments. My wife has been to Catalina a few times yet never heard of the Foxes.

  23. Paul S
    Posted April 28, 2016 at 4:27 pm | Permalink

    Very cool, this explanation of genetic drift helps with my general understanding of evolution.

    However, kitteh is not happy that you said she was obese.

  24. infiniteimprobabilit
    Posted April 28, 2016 at 5:48 pm | Permalink

    In the top photo, if I put the tip of my finger over the end of Mr Fox’s nose, he looks *exactly* like a kitteh. The ‘honorary cat’ title is well justified.

    cr

  25. Eduardo
    Posted April 28, 2016 at 5:52 pm | Permalink

    Very nice post!

  26. cherrybombsim
    Posted April 28, 2016 at 11:12 pm | Permalink

    Hmm. Seems like the tameness points to human introduction.

    One thing that occurred to me about the homozygosity and genetic drift, though: The population size of these foxes crashed for a couple of decades around 1990, to maybe 1/10 of their previous size.

    This is enough time for the genetic diversity to go way down, but it is not enough generations for slightly deleterious alleles to accumulate by neutral drift. It’s not like these populations were at that 1/10th size for 9000 years, which would prolly be pretty awful.

  27. Posted April 28, 2016 at 11:14 pm | Permalink

    In addition to an enlightening explanation and a *cute factor* that’s off the charts, I like that you sent me to the dictionary. “Depauperate” was the quest this time. Now I know!

  28. Dale Franzwa
    Posted April 28, 2016 at 11:37 pm | Permalink

    Great post, Jerry. But my interest is not in foxes or science but in fishing. In past years, I fished both S. Catalina and S. Clemente Islands (ocean) from the Southern Calif sportfishing fleet boats. At times, great fishing to be had here (Maybe S. Barnard might want to take note).

  29. Nick
    Posted April 29, 2016 at 2:43 am | Permalink

    At the risk of violating Da Roolz, please, please, PLEASE, don’t stop writing posts like this one, even if it does attract fewer comments than other non-science related posts. I loved it – thanks Jerry.

  30. Dominic
    Posted April 29, 2016 at 3:21 am | Permalink

    Interesting! And that they may have been deliberately introduced…

  31. ChrisH
    Posted April 29, 2016 at 8:00 am | Permalink

    Very cute.

    As I live in London I see urban foxes pretty much daily. At least one of them in my neighbourhood is very friendly (will come right up to you if there’s a fence in the way, happy to maybe 4ft if not). Still, they have been known to go after cats & other pets.

  32. Posted April 29, 2016 at 8:41 am | Permalink

    Very cool, thanks for this.

  33. Jonathan Wallace
    Posted April 30, 2016 at 4:12 am | Permalink

    “…and if those pressures sufficiently reduce mortality or reproduction, a species with very low genetic variation might go extinct.”

    Presumably that should be “either increase mortality or reduce reproduction…”?

    Great post. Really interesting.


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