When a small population becomes isolated by moving to a new location it is called?

Darwin’s greatest achievement was explaining how one species evolves over time, but it was not until the 1930s that biologists seriously addressed the other big problem of biodiversity: how does a single species divide into two or more lineages? The answer has involved a recurrent controversy: does that splitting, or speciation, require that populations be geographically isolated, or can species split in situ? A paper by Papadopulos et al. in PNAS (1) supports the latter idea, shedding light on the role of biogeography in speciation.

Speciation that occurs in a small area, with populations exchanging genes as they begin to diverge, is called sympatric speciation. Although this idea was popular in the early 20th century, critics like Mayr (2) suggested, and theory later confirmed (3), that the sympatric formation of two reproductively isolated groups—Mayr’s biological species—was difficult (2), for gene flow between populations can overcome evolutionary forces like natural selection that pull them apart. (Sympatric divergence is less difficult if a population can adapt to different ecological niches in the same area.) But speciation becomes much easier when diverging populations are geographically isolated (allopatric speciation), because in such cases there is no gene flow to prevent the accumulation of evolutionary differences whose byproduct is reproductive isolation.

Allopatric speciation is not controversial: there are many species that clearly formed in geographic isolation, including single endemics on islands and sister species (each other’s closest relatives) on opposite sides of geographic barriers (4). However, it is much harder to find examples of speciation that happened while the nascent species were exchanging genes, for even if sister species now occupy the same area, they could have originally speciated in allopatry and then expanded their ranges. With the exception of polyploidy (the formation of new species by chromosome doubling in pure species or interspecific hybrids), there are few uncontested cases of sympatric speciation (3).

Papadopulos et al. (1), however, use a method designed to increase the likelihood of identifying such cases: one simply surveys species in areas, like isolated oceanic islands and tiny lakes, where the geographic isolation of populations was always unlikely. If one finds endemic sister species in such places, then they probably formed there (3). The isolated island method has already uncovered several species of cichlid fish that likely formed in tiny volcanic crater lakes (5, 6) as well as two species of palms that diverged on a South Pacific Island (7).

The work of Papadopulos et al. (1) takes this approach a step farther by surveying the entire flora of a small, isolated island, searching for endemic sister species that could have formed in situ. Surprisingly, they find an appreciable number of species that fill the bill (1).

Their study site is, in fact, Lord Howe Island (LHI), home of the sister species of palms mentioned above. LHI (Fig. 1A) is a volcanic island between Australia and New Zealand that is roughly 6.9 Myr old. With an area of about 16 km2, it is sufficiently small that it would be hard for populations of an ancestral plant, particularly one pollinated by wind, to become geographically isolated. As Papadopulos et al. (1) note, the LHI flora comprise 242 species in 179 genera. Seventeen of these genera include at least two species endemic to LHI, which are, therefore, candidates for sympatric speciation. To determine whether any endemics were sister species, Papadopulos et al. (1) use molecular-based phylogenies, which can distinguish sympatrically formed relatives from those arising through double colonization, an allopatric process producing two related but nonsister species that arise after two invasions of ancestors from other areas.

(A) Lord Howe Island (image courtesy of Ian Hutton). (B and C) Two sister species of endemic palms that likely arose sympatrically on Lord Howe Island: Howea forsteriana (B) and H. belmoreana (C). Images courtesy of William Baker.

Pinpointing sister species requires molecular phylogenies not just of species on LHI, but, ideally, of every species in the 17-candidate genera—clearly an impractical task. Papadopulos et al. (1) do a creditable job, using previously published DNA sequences, generating their own sequences from both nuclear and chloroplast genes, and achieving coverage ranging from 7% to 100% of the species in different genera.

Although the sympatric Howea palms of LHI (Fig. 1 B and C) were described before (7), the analysis by Papadopulos et al. (1) adds at least nine more species that seem to have arisen from common ancestors on the island. These include five species in the genus Coprosoma, two in the genus Metrosideros, and two in the fern genus Polystichum. These 11 species imply that at least 4.5% of LHI flora arose by sympatric speciation. This figure is convincing, because the phylogenies of all four genera involved between 80% and 100% of all congeneric species from both LHI and other areas likely to produce colonists.

By including genera in which molecular phylogenies involve a smaller percentage of the congeneric species (16–54%), Papadopulos et al. (1) find nine more species that may have resulted from sympatric splits on LHI: two species in the genus Alyxia, two in Geniostoma, and two and three species, respectively, in the fern genera Grammitis and Asplenium. These cases, however, are more doubtful: incomplete phylogenies may miss some true sister species that live in other places, invalidating some examples of sympatric speciation.

Nevertheless, if we include all 20 species, as many as 8.2% of LHI plant species arose through splitting events on the island. This figure compares with 24.8% of LHI plant species formed allopatrically (e.g., single endemics on the island) and 55.4% of LHI plant species that did not speciate (LHI species also found elsewhere). Therefore, although allopatric speciation is still the largest contributor to endemic diversity on LHI, the discovery of an appreciable fraction of speciation events involving sympatry will surprise some evolutionary biologists. It also suggests that similar levels of sympatric speciation might occur on continents but in those places it is simply more difficult to rule out the allopatric alternative.

What is even more surprising is that 14 of the sympatrically formed species on LHI are either wind-pollinated or, if ferns, have wind-dispersed spores, suggesting high gene flow that would seem to make sympatric speciation harder. Less startling is the observation that—as theories of sympatric speciation predict—the endemic sister species of LHI are ecologically different, adapted to different local habitats and altitudes, or flowering at different times.

How much confidence can we place in the conclusions of the work by Papadopulos et al. (1)? One might discount the nine species whose phylogenies involved less than 60% of the genus, but that omission still leaves nearly 5% of the LHI flora as candidates for sympatric speciation. A more serious worry is that some of the phylogenies (involving 9 of 20 species, including 2 of the best-supported 9 species) were based only on DNA from chloroplasts—organelles that can, through hybridization, move between plant species far more readily than can DNA from the nucleus. This differential movement can produce discrepancies between phylogenies based on nuclear vs. chloroplast genes (8). For some LHI plants, then, their genetic status as sister species might be spurious, reflecting not true evolutionary relatedness but simply the movement of chloroplasts through hybridization. However, this omission still leaves at least nine species whose sympatric origin is strongly supported by both types of DNA.

It is worth noting that similar studies from other groups have shown much less evidence for sympatric speciation. Biogeographic work on birds and lizards has failed to turn up a single case of sister species on small islands (9, 10); similar conclusions come from a recent survey of several animal and plant groups (11). In response, Papadopulos et al. (1) suggest that “speciation in the face of strong gene flow may be a botanical specialty.”

Finally, it is worth emphasizing that, although the LHI plants may have speciated sympatrically in the biogeographical sense (12)—that is, in a small area—they may not have speciated sympatrically in the population genetic sense—that is, in the face of initially free gene flow between speciating populations (13). In several cases of biogeographical sympatric speciation, plant and animal species have special genetic or behavioral tricks that, by strongly reducing gene flow from the outset, allow populations to diverge in a small area. These cases include both auto- and allopolyploidy (not seen in any of the LHI cases), diploid hybrid speciation (seen in one LHI species), behavioral imprinting of avian nest parasites on hosts (14), and speciation involving rapid nongenetic changes in phenology that accompany movement to a new habitat. Indeed, the last process may have promoted speciation in the LHI Howea palms, because the ancestor of one species colonized drier soils that environmentally induced earlier flowering, instantly reducing gene flow with populations on wetter soil. Because the term sympatric speciation can be used in either a geographic or genetic sense, it may be better to simply drop the term, classifying modes of speciation solely on the levels of gene flow between incipient species (13).

Surveys of oceanic islands like Lord Howe are perhaps our best way to estimate how often speciation occurs with gene exchange. The bonus is that there are dozens of oceanic islands suitable for this kind of work. Equally promising material can be found in hosts and their parasites. A host species, after all, can be seen as an island for its parasites, and the discovery of endemic sister species of parasites on a single species of host would suggest speciation with gene flow (3). All of these studies, however, require laborious phylogenetic analysis of entire groups, surveys that must go beyond the chloroplast and mtDNA that, readily exchanged between closely related species, can yield misleading trees. Fortunately, rapid growth in both sequencing methods and bioinformatic analysis has made nuclear DNA an increasingly viable option.

The data of Papadopulos et al. (1), combined with those data from other island-dwelling plants and animals, suggest that speciation with gene flow is neither impossible nor common. But the work has just begun.

Footnotes

The author declares no conflict of interest.

See companion article on page 13188.

References

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