Bipolar biogeography.

I n PNAS, Popp et al. (1) present a convincing molecular phylogenetic analysis of a small group of ericaceous flowering plants, Empetrum (the crowberries), which includes species distributed at high northern latitudes and high southern latitudes but nowhere in between—a so-called bipolar (or antitropical or, broadly speaking, amphitropical) disjunction (Fig. 1). They contend that the best explanation for this distribution is that, sometime during the MidPleistocene, a bird—perhaps a Whimbrel— ate the fruits of an E. nigrum plant, probably living in Alaska, and then flew to the southern tip of South America before depositing the seeds (1). At first blush, this sounds like the sort of trivia that you might find on a natural history blog. Why are we reading about this in PNAS? In what context could such a one-off historical accident possibly be of any general scientific interest? The answer, as I will develop, concerns the bipolar nature of biogeography itself. Let us begin with Charles Darwin. Darwin devoted 2 of his 15 chapters in The Origin of Species (2) to biogeography, because he recognized the importance of explaining geographic distributions to his entire argument on evolution. It would seriously undermine the continuity of evolution if the same species could spring into existence in separate areas. Very wide geographic disjunctions seemed, to some at least, to negate the central idea that species stem from a common ancestor that originated atjust one point in time and space. How, then, could the most challenging disjunctions—the bipolar ones—be explained in evolutionary terms? In the sixth edition of The Origin of Species, published in 1872, Darwin included a section entitled “Alternate Glacial Periods in the North and South” in which he developed an explanation for bipolar distributions that relied on nothing more than the normal migration of species in response to climate change (2). His explanation took advantage of newly emerging ideas on glacial cycles, which suggested that a glacial period in the north would correspond to an interglacial period in the south. Darwin saw in this glacial seesaw a pumping mechanism. During cold periods in the north, cold-adapted species would move south, where they would comingle with more tropical elements. When it warmed up, some of these plants would move up into any nearby mountains, say the Andes. Likewise, when the south next cooled, southern organisms would move north and then south again as cold climates receded, but this time, “carrying southward with them some of the northern temperate forms which had descended from their mountain fastnesses” (2). Ingenious! Alfred Russel Wallace, even more the biogeographer, developed his own take on bipolarity. In Island Life, published in 1880 (3), he agreed that plants had moved mainly from the north but not by Darwin’s pump. Instead, during glacial periods, when tree-lines were depressed, he envisioned plants mountain-hopping southward along the Andes (3). As for missing elements in the Andes today, Wallace reasoned that “we may connect their disappearance with the passing away of the last glacial period which, by raising the snow-line, reduced the area on which alone they could exist” (3). In a letter to Wallace, Darwin expressed his doubt: “This is rather too speculative for my old noodle. I must think that you overrate the importance of new surfaces on mountains and dispersal from mountain to mountain”. The Darwin and Wallace hypotheses differed in detail, but both envisioned the migration of plants during recent glacial periods, mainly from the north to the south, and neither of them invoked longdistance dispersal from one area all the way to the other. However, fast-forward 80 years to Peter Raven’s classic paper on amphitropical plant distributions (4), and long-distance dispersal becomes the leading explanation. In part, Raven (4) based this argument on new lines of evidence, such as the preponderance of self-compatibility in bipolar plants (“Baker’s law”) (5), their lack of specialized pollinators, and their occupation of open habitats, all popular themes in the analysis of island colonization (6). Just then, however, the field of biogeography was on the verge of a revolution, brought on by the rise of phylogenetic systematics (7) and the emergence of socalled vicariance biogeography (8). This entailed the rejection of one-off biogeographic stories, and the search, instead, for general biogeographic patterns in cladograms that showed relationships among areas of endemism. General patterns implied the existence of general causal mechanisms, which were sought in earth history events, especially continental moments. Dispersal of any sort was viewed as an explanation of last resort, and longdistance dispersal was basically dismissed as unscientific (9). Therefore, bipolar disjunctions required another explanation and were soon interpreted as reflecting the breakup of the supercontinent Pangea (10). If this were the cause of bipolar disjunctions, then the relevant phylogenetic splits would date to the Mid-Jurassic or early Cretaceous, roughly 170–140 million years ago. Put in these terms, the choice between the major hypotheses could be made just by dating the relevant phylogenetic splits. Fig. 1. (Left) E. nigrum (reprinted from ref. 21). (Right) Map showing the Popp et al. (1) finding that the red-fruited southern species, E. rubrum (image courtesy of Arthur Chapman), originated from E. nigrum (image courtesy of Atli Arnarson) in northwestern North America with black fruits, not from red-fruited E. eamsii in Eastern North America. Specific collection localities were obtained from the Global Biodiversity Information Facility (http://www.gbif.org/). (Figure prepared by Jeremy Beaulieu.)