August 2002
Large-blotched Salamander, an Ensatina subspecies, of California. Source: Chris Brown, USGS.
To understand how evolution has produced the diversity of life, we need to study two fundamental processes:
- How a single species changes through time.
- How a single species becomes two or more species.
The first process has been observed and studied extensively in many species, for example in evolving beak sizes of Darwin’s finches1 and in evolving body sizes and developmental rates of guppies.2 The second process, called speciation, is more difficult to observe directly, primarily because it usually takes much longer than a biologist’s lifetime to occur.
Geography and speciation
One way to study speciation indirectly is to examine geographical variation, or how the characteristics of organisms differ between different locations. We can then infer from the variation how speciation occurs. During the early 20th century, biologists such as David Starr Jordan3 and Ernst Mayr4 used this approach and noticed that, in most cases, two closely related species do not occur at the same location nor are they distantly separated. Rather, they usually occur in geographically adjacent regions that are separated by a geographical barrier such as a mountain range or a body of water. The biologists concluded from this pattern that:
- Speciation often begins when a single species becomes geographically separated into two populations. Individuals cannot travel between the populations, preventing the two populations from interbreeding.
- Because the two populations cannot exchange genes, and because they may be subject to different environmental conditions, they slowly evolve differences.
- Eventually the two populations become different enough that they do not interbreed even if they come into contact (in other words, they are ‘reproductively isolated’), and are therefore separate species.
These conclusions were based on broad patterns in the distribution and relationships of many species. But determining how speciation occurs in any particular case can be difficult, because we are usually only presented with the outcome of the process (two species) and we often have no record of their common ancestor or the intermediate forms that occurred during speciation.
Ring species
Ring species provide unusual and valuable situations in which we can observe two species and the intermediate forms connecting them. In a ring species:
- A ring of populations encircles an area of unsuitable habitat.
- At one location in the ring of populations, two distinct forms coexist without interbreeding, and hence are different species.
- Around the rest of the ring, the traits of one of these species change gradually, through intermediate populations, into the traits of the second species.
A ring species, therefore, is a ring of populations in which there is only one place where two distinct species meet. Ernst Mayr4 called ring species “the perfect demonstration of speciation” because they show a range of intermediate forms between two species. They allow us to use variation in space to infer how changes occurred over time. This approach is especially powerful when we can reconstruct the biogeographical history of a ring species, as has been done in two cases.
Ensatina salamanders
One well-studied ring species consists of salamanders in the Ensatina eschscholtzii group, distributed in mountains along the west coast of North America. In 1949, Robert Stebbins5 described a fascinating pattern of geographical variation in these salamanders:
- Two distinct forms of Ensatina salamanders, differing dramatically in color, coexist in southern California and interbreed there only rarely.
- These two forms are connected by a chain of populations to the north that encircles the Central Valley of California, and through this ring of populations the color patterns of the salamanders change gradually.
Stebbins thought that this situation arose when an ancestral population of salamanders, in northern California, expanded southward along two fronts, one down the Sierra Nevada mountains, and the other down the coastal mountains. The two groups gradually became different as they moved south. When they met again in southern California, the two expanding fronts were so different that they rarely interbred, and were therefore different species. More recently, a team of researchers led by David Wake6-8 has examined genetic relationships among salamander populations using DNA sequences and other molecular traits, and the genetic evidence has supported Stebbins’ hypothesis. The geographical variation, when combined with the inferred history revealed by the molecular traits, allows us to envision the small steps by which a single ancestral species in the north gave rise through evolutionary divergence to two species in southern California.
Greenish warblers
Another ring species that has provided valuable insights into speciation consists of the greenish warblers (Phylloscopus trochiloides). These small, insect-eating songbirds breed in the forests of central and northern Asia and eastern Europe. In the center of Asia is a large region of desert, including the Tibetan Plateau and the Taklamakan and Gobi Deserts, where the warblers cannot live. Instead, they inhabit a ring of mountains surrounding this region, as well as the forests of Siberia to the north. The warblers have remarkable geographic variation:9-11
- In Siberia, two distinct forms of greenish warblers coexist, one in the west and one in the east, their distributions narrowly overlapping in central Siberia, where they do not interbreed. These forms differ in color patterns, the songs that males sing to attract mates, and genetic characteristics. Also, males of each form usually do not recognize the song of the other form, but respond strongly to their own.
- The traits that differ between the two Siberian forms change gradually through the chain of populations encircling the Tibetan Plateau to the south.
- Thus two distinct species are connected by gradual variation in morphological, behavioral, and genetic traits.
Claude Ticehurst,9 who during the 1930s studied variation in museum specimens of greenish warblers, hypothesized that the present pattern of variation arose when an ancestral species in the south, perhaps in the Himalayas, expanded northward along two pathways, one on the west side of Tibet and the other on the east. The two expanding fronts gradually became different, resulting in two distinct Siberian forms. More recently, studies of genetic variation and song variation have strongly supported this view.10-11
The pattern of song variation is particularly interesting:
- Songs are short and simple in the south, but to the north songs become gradually longer and more complex along both pathways into Siberia.
- However, songs have also become different in structure, resulting in distinct differences in songs between the Siberian forms.
The birds distinguish between these differences; males respond aggressively to tape recordings of their own songs, thinking that another male has invaded their territory, but they do not respond to songs of the other form. In most species of songbirds, songs play an important role in mate choice; usually, only males sing, and females listen to songs when deciding which male to choose as a mate.12 Speciation is essentially the evolution of reproductive isolation between two populations, and song differences can cause reproductive isolation. Hence, the geographical variation in songs of greenish warblers provides a rare illustration of how gradual change in a trait can cause speciation.
Demonstrations of evolution
Greenish warblers and Ensatina salamanders illustrate three fundamental ways that ring species can teach us about evolution:
- Ring species provide strong evidence for evolution causing the appearance of new species, demonstrating that many small changes can eventually accumulate into large differences between distinct species. Some critics of evolutionary theory think that evolution can only cause limited change within a species and cannot lead to the evolution of new species. Ring species show that they are wrong; variation between species is qualitatively similar, though different in degree, to variation within a species.
Ring species allow a reconstruction of the history and causes of divergence during speciation, since spatial variation may illustrate change through time. Without the rings of populations connecting the terminal forms, we would have little understanding of the history of divergence of greenish warbler songs or Ensatina color patterns.
Ring species provide evidence that speciation can occur without complete geographic isolation. As discussed at the beginning of this article, the prevailing view of speciation has been that two populations must become geographically isolated, such that they do not exchange genes, before speciation can occur (this process is called ‘allopatric speciation’). Ring species, however, show that the ends of a long chain of interbreeding populations can diverge to the point that they do not directly interbreed, even though genes can travel between them through the intermediate populations (in other words, they are connected by ‘gene flow’). This aspect of ring species has been rather controversial, and critics have argued that some apparent examples of ring species, such as Ensatina, have breaks in gene flow.13
Rarity of ring species
Since we can learn so much from ring species, it is unfortunate that few examples are known. At least 23 cases have been proposed, but most of them are not such clear examples as the salamanders and warblers.14 Most of the proposed cases have major gaps in distribution in the chain of populations connecting the terminal forms, and some cases appear to have more than one species boundary in the ring of populations. However, most of the cases have one thing in common: in one place, there are clearly two species, while in another area the boundary between species is difficult to determine.
Ring species are rare for several reasons:14,15
Their formation requires unusual geographic situations, in which a species can expand around a geographic barrier through a continuous ring of suitable habitat. The range expansion must occur slowly enough that the two expanding fronts have time to diverge before they meet on the other side of the barrier, and the size of the barrier must be large compared to the distance that individuals disperse.
The taxonomic rules that are used by biologists to classify organisms create a bias against recognizing ring species. Under these rules, a ring species must be classified either as a single species or as two species. Both classification schemes conceal the fact that there is gradual variation between reproductively isolated forms.
Ring species might be rare because many of them were destroyed before they could be discovered, as will be described below.
Importance of conservation
While ring species teach us about evolution, they also provide lessons about the importance of habitat conservation. They demonstrate that species can differ substantially between different parts of their ranges. Ensatina salamanders and greenish warblers are each usually classified as a single species, even though each contains populations that differ at the between-species level. As the commonly-used phrase ‘endangered species’ reveals, most conservation efforts are directed at the species level, and species are often eliminated from much of their range before they receive legal protection. However, within-species variation is an important component of biodiversity. Whenever a species is eliminated from part of its range, unique traits that were only found in that area are lost forever. Not only are the species and its traits lost from that area, but the particular story of evolution that could be learned from it is lost as well.
It is not a coincidence that the best two examples of ring species are both found in relatively undisturbed mountainous habitat. Ring species might have existed at one time in habitats such as the grasslands of central North America, but those would now be destroyed or severely altered because of the impact of agriculture. Large areas of greenish warbler habitat are being deforested, particularly in China, India, and Nepal, and this process might continue to the point that future biologists would not be able to recognize greenish warblers as a ring species. Undoubtedly, many undiscovered ring species are being destroyed now because of human activity, and many more will be lost in the future if we fail to protect their habitats.
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