Any kind of RIB reduces the amount of gene flow between species, but combinations of mechanisms result in the tightest isolation. Most ‘good’
species are separated by multiple combinations of RIBs. For example, the leafy-stemmed Gilia of central California, Gilia millefoliata and Gilia capi- tata,are isolated in five ways according to Grant (1963):
1) Ecological isolation: G. capitataoccurs on sand-dunes and G. millefoliata on flats. 2) Floral: G. capitatais large-flowered and bee pollinated, while G. millefoliatais small flowered and self-pollinating … 3) Seasonal isolation:
G. millefoliatablooms earlier than G. capitata. 4) Incompatibility: Hybrids are very difficult to produce by artificial crosses in the experimental garden.
5) Hybrid sterility: The F1s when they can be obtained are chromosomally sterile to a high degree, producing only about 1 percent of good pollen grains and no F2seeds.
Another clear example of multiple RIBs is found in crosses between P. vulgarisand P. coccineus. They rarely hybridize in the first place because they have different habitats (as mentioned earlier) and, when they do cross, there is poor seed set and high seedling mortality and the surviving hybrids have a ‘crippled’ morphology, represented by dwarfism and abnormal development. In addition, the F1s produce only a low propor- tion of viable gametes (Hucl and Scoles, 1985). In cases like these, it is highly unlikely that any successful hybridization will occur at all, even if the species are in proximity.
Other important criteria used to describe speciation pathways are:
(i) how large the speciating groups are; and (ii) how much genetic differenti- ation precedes the formation of strong RIBs. Allopatric speciation is broken into two groups – geographical and peripatric. In geographical speciation, large populations are thought to gradually diverge and form RIBs, while, in peripatric speciation, isolating barriers are thought to appear quickly in small populations without much differentiation. Sympatric speciation occurs when a single individual or small group arises that is reproductively isolated from the surrounding population. Parapatric speciation is closely related to sym- patric speciation, except that the gradually diverging crowd of genotypes is on one side of the parent population rather than surrounded by it.
Numerous other speciation taxonomies have been proposed (White, 1978; Templeton, 1981), but the five depicted in Table 5.4 are the ones most commonly discussed in the evolutionary literature. We shall describe synonyms and related concepts in the text where appropriate.
Geographical speciation
The most widely recognized type of speciation is geographical speciation. In its first stage, there is a single population found in a large homogeneous envi- ronment. The environment then becomes partly diversified due to physical or biotic factors and populations become isolated. These populations begin to diverge genetically and eventually acquire sufficient variation to become reproductively isolated from each other (semispecies). Further changes in the environment allow some of the newly evolved groups to come back in con-
Allopatric
Parapatric Sympatric Geographical Peripatric
Types of gradual speciation
Freely interbreeding population
Establishment of subpopulations via environmental or
geographical substructuring Genetic differentiation leading to partial RIBs Reunification and strengthening of RIBs
Fig. 5.6. Cartoons illustrating the different modes of gradual speciation. The drawings found below each of the individual headings (geographical, peripatric, parapatric and sympatric) represent the various stages of species development. See the text and Table 5.4 for more details.
tact, but they do not produce successful hybrids because of past differentia- tion. Natural selection against the formation of weak or sterile hybrids pro- motes the reinforcement of RIBs through additional differentiation.
Most of the evidence for this type of speciation is circumstantial in nature due to the slow speed of the process. Few scientists’ careers are long enough to follow the whole scenario. However, populations in the various stages of speciation have been identified by individual investigators. Probably the most complete story in plants has been accumulated by Grant and Grant (1960) in their oft cited Gilia studies. In this group, they were able to find races and species in all the hypothesized stages of geographical and ecological differen- tiation (Fig. 5.7), and they were able to show a subsequent build-up of isolat- ing mechanisms as the species became more divergent (Table 5.5).
Peripatric speciation
This type of speciation is very similar to the geographical mode except the speciating population is much smaller. Other terms used for this type of spe- ciation are quantum (Grant, 1971), speciation by catastrophic selection (Lewis, 1962) and founder-induced speciation (Carson, 1971; Carson and
Contiguous geographical races
Disjunct geographical races
Contiguous semispecies Contiguous species G. latiflora
excellens davyi cuyamensis
latiflora
G. leptantha
purpusii
pinetorum transversa leptantha
G. ochroleuca G. tenuiflora,
leptantha, and latiflora G. leptantha
G. latiflora G. tenuiflora
Fig. 5.7. Populations and species of Giliarepresenting different stages of allopatric speciation (redrawn with permission from V. Grant, © 1963, The Origin of
Adaptations, Columbia University Press, New York).
Templeton, 1984). Because of reduced population size, genetic drift becomes more important and the rate of speciation is accelerated. Peripatric speciation can result in reproductively isolated species that are otherwise quite similar to their progenitors or they may become morphologically quite distinct, depending on how many genes are affected. Most of the evidence for peripatric speciation is also circumstantial, although the process can occur during the lifetime of an individual investigator.
One of the most completely documented cases of peripatric speciation associated with few genetic changes concerns two Clarkiaspecies in south- ern California (Lewis, 1962). Clarkia bilobais a relatively widely distributed species, while Clarkia lingulata is rare and is found on only two sites at the extreme edge of the C. biloba range. The two species are very similar elec- trophoretically and morphologically except for flower petal shape (Fig. 5.8);
however, they are reproductively isolated by a translocation, several para- centric inversions and a chromosomal fusion. Lewis suggested that C. biloba arose when an isolated C. lingulatapopulation crashed during a drought to only a few individuals, which by chance contained the chromosomal rearrangements. The cultivated rye, Secale cereale, may also have arisen via parapatric speciation from the wild species, Secale montanum. The two species vary by two reciprocal translocations and are reproductively isolated, but in most other respects are similar. White (1978) uses the term ‘stasipatric speciation’ to describe the formation of new species due to the fixation of chromosomal rearrangements.
The dramatic reduction of a population due to an environmental cata- strophe or the establishment of a ‘founder population’ of a few individuals can also lead to a morphologically distinct species when the remaining sam- Table 5.5. Relative ease of crossing diploid cobwebby Gilia at different levels of
divergence (from Grant and Grant,1960).
Number of Average no. Number of hybrid flowers plump seeds individuals per ten Type of cross Entities crossed pollinated per flower flowers pollinated
Interindividual Different individuals 116 17.8 22
belonging to the same population
Inter-racial Different geographical 562 15.2 12
races of the same species
Interspecific Different diploid species of 2016 3.7 3 cobwebby Gilia
Intersectional Diploid species of cobwebby 528 0.004 0.032 Giliawith diploid species of
leafy-stemmed or woodland Gilia
ple of the gene pool is unbalanced and ‘undergoes a genetic revolution’
(Mayr, 1954) or ‘genetic transilience’ (Templeton, 1981). Genetic drift and changes in selection pressure can result in a shift of many genes into new coadapted complexes. A wide range of distinct plant and animal species in the Hawaiian islands are thought to have arisen in this manner (Carson and Templeton, 1984). The most thoroughly documented cases involve repre- sentatives of the Drosophila, but the silversword alliance of the Compositae includes giant herbs, small trees and ecologically diverse shrubs (Carr and Kyhos, 1981). Small founder populations do not always undergo dramatic alterations, however, as most of our crop species are based on relatively few genotypes and still retain a strong resemblance and interfertility with their progenitors (Chapter 7).
Parapatric speciation
In this mode of speciation, RIBs evolve without geographical separation.
The diversifying population is adjacent to the progenitor population (neigh- bouringly sympatric (Grant, 1985)). The process occurs when a subgroup diverges in response to environmental challenges and isolating barriers begin to form as a by-product of ecological differentiation.
Whether populations can diverge sufficiently without geographical sepa- ration has long been a matter of debate. Mayr (1942, 1963) contended that portions of populations are unlikely to differentiate enough to become Fig. 5.8. Morphology, cytology and geographical range of Clarkia biloba(A) and its peripatric derivative species Clarkia lingulata(B) (used with permission from H.
Lewis, 1962, Evolution16, 257–271).
genetically isolated in the face of strong gene flow. This would be particu- larly true among sympatric subgroups where the diverging race is completely contained within the parent population and is bombarded on all sides by pollen and seed. There are, however, numerous examples where parapatric populations have undergone substantial differentiation in the face of one- dimensional gene flow. We have already described the mine-tailing experi- ments of Bradshaw where the differentiated populations varied not only in heavy-metal tolerance but also in flowering date (Chapter 2). McNeilly and Antonovics (1968) have catalogued numerous similar scenarios where eco- logically divergent populations have different bloom dates (Table 5.6).
Artificial selection experiments have also shown that relatively strong RIBs can arise over a few generations when strong selection is placed on unre- lated characteristics. Paterniani (1969) planted white flint and yellow sweet maize in the same field together. Each generation, he selected the purest ears for subsequent planting and, after six generations, fewer than 5% of the seeds resulted from an outcross (Fig. 5.9). These experiments demonstrate that parapatric speciation is at least theoretically possible; it is up to the field biologists to document the complete process in nature.
Sympatric (instantaneous) speciation
Occasionally, new species arise through spontaneous mutation without any ecological or geographical separation. A new isolated type appears in only a few generations without substantial genetic differentiation. Most of these types face a high likelihood of rapidly becoming extinct due to their low numbers, but, even against these odds, many species are known to have had their origin in this manner. Probably the most frequently cited example of sympatric speciation occurred in the apple maggot, Rhagoletis pomonella (Bush, 1975). The original host plant of R. pomonella in the USA was hawthorn (Crataegus), but the fruitfly began to infest introduced populations of apples in the mid-1800s. Apparently, there was a change in a single gene trait affecting host recognition that isolated the two populations with minimal genetic change. The genus Rhagoletis has a large number of very similar species that infest fruits of different plant families.
R. pomonella– Rosaceae R. mendax– Ericaceae R. carnivora– Cornus R. zephyria– Caprifoliaceae
Examples of instantaneous speciation abound in plant species. We have already discussed polyploidy at length, where a chromosomal duplication instantly isolates a progeny plant from its parents; at least half of all plant species are polyploid. Even the appearance and fixation of simple chromo- somal rearrangements can result in a new species. Stephanomeria mal-
heurensis is a self-compatible species that was probably derived from the self-incompatible Stephanomeria exigua subsp. coronaria (Gottleib, 1974, 1977b). They are morphologically and electrophoretically quite similar and share a single habitat, but S. malheurensiscarries a chromosomal transloca- tion that reproductively isolates it from S. exigua. The appearance of self-
Table 5.6. Differences in flowering time of ecotypes compared with the ‘normal’ type (from McNeilly and Antonovics, 1968).
Flowering species Ecotype Time
Gilia capitata Sand dune Later
Madia elegansa Subsp. vernalis Spring Subsp. aestivalis Summer Subsp. densifolia Autumn
Layia platyglossaa Maritime Later
Hemizonia citrinaa April
Hemizonia lutescensa Aug.–Sept.
Hemizonia luzulaefoliaa April
Hemizonia rudisa Aug.–Sept.
Lactuca graminifoliaa Early spring
Lactuca canadensisa Summer
Ixeris denticulata Subsp. typica Spring Subsp. sonchifolia Autumn Subsp. elegans Summer
Pinus attenuataa Later
Pinus radiata Earlier
Lamium amplexicaulea Vernal race Earlier
Viola tricolor Sand dune Later
Silene cucubalis Earlier
Silene maritima Later
Geranium robertianum Shingle beach Later
Mimulus guttatus Coastal Late
Mountain Latest
Valley and foothills Early
Geum urbanea Later
Geum rivalea Earlier
Succisa pratensis Northern race Earlier
Ranunculus acer Alpine Earlier
Solidago virgaurea Alpine and coastal Earlier
Rumex acetosa Alpine Earlier
Leontodon autumnale Coastal Earlier
Clarkia xantianaa Self-compatible race Earlier
Salvia mellifera Early spring
Salvia apiana Late spring
aSome evidence given by author that ‘ecotypes’ are adjacent.
compatibility in the new type probably allowed the translocation to become homozygous through selfing rather than being lost in an outcrossed flood of parental chromosomes.