Genetic divergence under selection can be classified into two major geographic modes:
1. Local disruptive selection - sympatric divergence
Divergence in "sympatry",
or within the "cruising range", or
dispersal range of a single population. Examples
are "host races" of host-specialist parasites.
2. Geographically varying selection (or drift)
a) Parapatric divergence
Divergence in "parapatry",
spatially separated populations
that remain in contact at the
boundary. An example is the
divergence in melanism of the
peppered moth between
Liverpool and North Wales.
b) Allopatric divergence
Divergence in "allopatry",
in separate populations that
are not in contact. Clearly
occurs in many island
Geographic distributions: obviously, allopatric divergence may result in parapatric distributions via secondary contact. The reverse is also possible; allopatric distributions could result from the abolition of a contact zone between parapatrically distributed forms. Thus, you cannot tell much about the geographical mode of origin of a distribution just from the current distribution.
Genetic divergence and speciation
Necessarily, speciation involves genetic divergence; for any extant pair of species, this divergence has taken place at some past time. We cannot usually study the genetic history of speciation directly, because we only have access to present-day populations. However, we can study spatial variation in gene frequencies. Because dispersal is spatially limited, distant populations share ancestry less recently than adjacent populations, and so, to some extent, spatial variation represents temporal variation in gene frequencies. By studying spatial variation, we may be able to come to some understanding of the time course of genetic divergence and speciation.
Many newly formed pairs of species have
parapatric or allopatric distributions. Parapatric distributions and contact
zones within species in particular are very interesting to evolutionists
because they represent a first step in speciation. Because all intermediates
between slight genetic differentiation and separate species occur in parapatry,
we can use these examples to study the time course of speciation. The remainder
of the lecture will concern this class of distributions.
Genetic variation across a geographic area
Any consistent change in gene frequency, or in heritable phenotype, across the geographical range is known as a cline. Clines occur because dispersal across a region is limited, because the whole geographical area does not form a single panmictic population. (Population geneticists often call dispersal migration, though they do not at all mean the same thing as ecologists; for instance, we do not mean the kind where birds return after migration to near their parents nest! We also use the term gene flow, though we usually mean genotype flow, when you think about it.). Because dispersal is not universal, other processes, especially genetic drift or selection can outweigh the homogenizing effect of the movement of genes. This can lead to a cline being maintained by a drift/migration balance, or a selection/migration balance. Genetic diversity may thus be maintained spatially, as already mentioned in maintenance of variation:
a) Clines produced by drift/migration balance
Random drift on its own will not produce consistent directional changes in gene frequency. (For details about evolution under conditions of patchy selection or drift, see the notes on population structure and gene flow and Futuyma 1998 pp. 297-298, 315-320. Due to time constraints this important subject can no longer be part of the course). However, locally, drift can result in a temporary monotonic change. Because drift is not usually very powerful unless local population sizes are small, drift will usually produce broad, random clines, which are prone to reversal over time.
b) Clines produced by selection/migration balance - EXTRINSIC selection
If selection favours different alleles in different areas, and if dispersal is not completely universal, it is fairly clear that gene frequencies may diverge and equilibrate in different parts of the range.
Extrinsic or environmental selection is imposed by the environment directly. If two types of environment favour different genes or phenotypes, if these two environments are sufficiently widely spaced, and if migration rates are not too high, it is easy to see that this will set up a cline in gene or phenotype frequency. We have already met an example of a cline maintained by extrinsic selection; can you remember what it was? (Peppered moths in rural North Wales versus urban Manchester and Liverpool). Another example is sickle-cell haemoglobin in malaria-infested vs. malaria-free areas of the world, clines in heavy metal tolerance in plants, and even clines in the frequency of insecticide resistance.
If the dispersal of an individual between place of birth and breeding site is essentially random, it resembles a "drunkards walk". You have probably encountered this sort of movement in physics already; it has the same distribution as passive diffusion, a two-dimensional normal distribution.
If this is true, dispersal distance can simply measured as the standard deviation, , of the dispersal distribution. A population "neighbourhood" can be defined approximately as a group of individuals who come from an area 2 wide.
[Strictly, is only a valid measure of dispersal if dispersal is exactly normally distributed. In practice, it doesn't much matter if dispersal is non-normal, provided it is not too extreme. (Many field studies have shown that dispersal is leptokurtic, i.e. most offspring breed very close to their parents, but some breed an enormous distance away.)]
Theory of clines under extrinsic selection
At equilibrium between gene flow and selection, the width of a cline (w = 1/[maximum gradient in the centre], see Fig.) is proportional to dispersal divided by the square root of selection. In fact:
w 1.7/sMore important than understanding how we get it is what this means.
First, it should, in retrospect, obvious that the width of a cline scales directly to dispersal distance; the cline will get wider as the dispersal increases.
Second, it is obvious that stronger selection across an environmental gradient should result in a narrower cline, i.e. w should be inversely proportional to some function of selection. So the equation seems more or less sensible, though the square root and the 1.73 comes out of the maths.
Also more important than understanding the maths is knowing why we want such an equation! It provides us with a way to understand the evolutionary phenomenon of clines.
This theory was used by Jim Bishop in 1972 to study the cline of melanism in the peppered moth between North Wales and Liverpool [SEE OVERHEAD]. Bishop obtained the cline theory by computer simulation rather than by the above analytical theory, but the principle is the same. He used a mark-release-recapture experiment to estimate selection and dispersal along the transect. He then compared the actual cline in melanism with the predicted cline based on his simulations of the computer results. Bishop found that the melanics reached further into pristine(?) North Wales than expected on the basis of the model; and explained this via a probable greater fitness of the melanics during the larval stage, which was not accounted for in his experiments of mark-recapture of adult moths.
[Adaptation to patches. In insecticide treatment, we might be able to use the information. For example, if we treat African villages with insecticides to prevent malaria transmission by Anopheles mosquitoes, and we knew the selection pressures and dispersal distance, we might be able to ensure that we avoid insecticide resistance in villages that are less than about 2w wide. This should work because two back-to-back clines cannot form over a village unless the area is sufficiently big relative to the widths of clines. (Unfortunately for this policy, many insecticides used in malaria control are also used in crop protection outside the villages, so that mosquitoes get treated even in rural areas where there is no need to treat with insecticides against malaria transmission. This means that Anopheles can adapt to insecticides over vast areas.).]c) Clines produced by selection/migration balance - INTRINSIC selection
i) Heterozygous disadvantage
Not all selection is dependent on the environment; selection may be completely intrinsic. We have come across a single locus example of this in heterozygous advantage and disadvantage acting on chromosomal rearrangements. Heterozygous disadvantage creates a kind of disruptive selection. The equilibrium gene frequency, t/(s+t) is unstable, with selection tending to prevent polymorphism. There are two peaks in mean fitness, known as adaptive peaks; fixation for A, and fixation for a. Thus most populations will end up fixed for one or other allele. Where they overlap, they will produce a narrow cline where the two populations mix, and where dispersal or mixing is balanced by selection against hybrids.
Perhaps surprisingly, this kind of intrinsic selection will produce clines with very similar shape to those found when extrinsic selection is operating. The constant of proportionality is different for different models of selection, but the equations describing shape and width will be very similar. Under heterozygous disadvantage,
w 2.8/s', ... where s' is an average of s and t.Again, it is fairly easy to understand the general feel of this equation: the stronger the selection, s, the narrower will be the cline. The greater the dispersal distance,, the more blurred and broader will be the cline.
ii) Frequency-dependent selection
Another example of intrinsic selection is frequency-dependent selection. Here, the strength of selection depends on the frequency of alleles in the population. An example is warning colour, where the commonest form is the fittest because it will presumably have already taught more predators to avoid the colour pattern. A rarer colour pattern will be attacked more. If colour patterns start off with different abundances in different areas, the region will stay patchy for the colour patterns, and, once again, clines under intrinsic selection will form between them. It turns out that frequency-dependent selection will result in almost exactly the same kinds of clines as for heterozygous disadvantage. Heterozygote advantage or disadvantage is, in fact, frequency-dependent at the genic level, when you think about it!
iii) Epistatic and disruptive selection
If the environment is constant, but selection is disruptive, there is a special case where intrinsic selection may be caused by the environment. Here selection may favour a bimodal phenotypic distribution, or two adaptive peaks simultaneously. For example, the Darwin's finches have available large, tough seeds, as well as small soft seeds, which are hard to get out of their pods or off grass stems. One type of seed selects for stout, deep beaks; the other for narrow pincer-like beaks.
Quantitative traits like beak width are usually controlled at multiple loci, and bimodal adaptive landscapes imply epistasis, or interactions in selection between genes. Suppose A and B both cause larger beaks, whereas alternative alleles a and b both result in smaller beaks. AA BB will have very large beaks, while aa bb will have very small beaks, both of which may be near the bimodal optimal beaks. Intermediates with Aa bb or Aa Bb, for example, will have beaks that "fall between two stools". The fitnesses at loci A and B depend on each other (which is the definition of epistasis) to produce optimal phenotypes. Thus disruptive selection produces epistatic selection, one of the potential causes of linkage disequilibrium (correlations between loci within genotypes). Disruptive selection of this kind isalso implicated in models of sympatric speciation (a couple of lectures from now), but it clearly could be important for generating divergence in parapatry.
Another and very important potential example of epistatic/disruptive selection is sexual selection and mating behaviour, in which genes for mate choice are strongly epistatic on genes for the traits being chosen. Clearly, epistatic genes in mating behaviour might cause speciation directly by altering mating patterns (see SPECIES AND SPECIES DIFFERENCES next time).
A bimodal phenotypic distribution is virtually impossible to maintain in/ a randomly mating population (because mendelian inheritance ensures that phenotypes at multiple loci are approximately normally distributed - see QUANTITATIVE GENETICS). Specialization on the second type of seed ruins adaptation to the first, and vice versa. In this case, selection sets up stresses which multiple loci cannot easily resolve. There are three solutions to this problem.
Polymorphism. A single locus or "supergene" polymorphism could evolve, such that each morph occupies a different habitat. This is unlikely in the case of a multilocus trait like size (but it is not unknown: in some fish, size is dimorphic due to a polymorphism at growth hormone receptor loci).Evolution of clines
Speciation. If there are actually two populations of different species, bimodality is easy to achieve overall by evolution in opposite directions in each species, because recombination between the forms does not occur. Competition, in fact, will usually ensure that already reproductively isolated species will diverge to form a bimodal pattern of habitat use overall (see SPECIATION in a few days). However, the selection against intermediates (or hybrids) within a single species will also act as a component of reproductive isolation. Thus, or parapatric sympatric speciation is a potential outcome of disruptive selection (see speciation lecture).
Loss of one adaptive peak. Normally, the population evolves to the most powerful adaptive peak or the other, because otherwise the majority, near the phenotypic mean, would suffer the consequences of poor adaptation to both hosts. Essentially, a "loss of the adaptive peak" means extinction of the population or species occupying that peak.
Any one of the various kinds of intrinsic modes of selection -- heterozygote disadvantage, frequency-dependent selection, or disruptive/epistatic selection -- can stabilize clines of gene frequency (in the case of epistasis, clines of more than one gene). Because all these types of selection are intrinsic, the clines they produce are also mobile, or at least not rooted to environmental gradients.
Under Ernst Mayr's "biological species
concept", species are reproductively isolated from one another. Intrinsic
and even extrinsic selection across clines gives a degree of "reproductive
isolation", in that crosses between the types produce poorly adapted heterozygotes
or other kinds of intermediate phenotypes. Knowing about spatial evolution
and cline theory is therefore important for understanding speciation.
Hybrid zones are narrow zones of contact between divergent forms or even species are found in parapatric distributions. Hybrid zones may include few hybrids or many, and the hybrids themselves may consist only of F1 only, or of F1, F2 and every kind of backcross.
Many species and/or races are distributed parapatrically, and have narrow hybrid zones between them. We have already seen examples in the case of chromosomal races of mammals, and grasshoppers, where heterozygote or hybrid disadvantage presumably maintain the clines. But we also see them for frequency-dependent traits like warningly coloured butterflies, sexually selected birds [SEE OVERHEAD OF PARAPATRIC MANAKINS IN COLOMBIA AND PANAMA], and for other morphological traits as well.
Hybrid zones are usually first noticed because they separate morphologically different races or chromosomal races, but further investigation shows these races often differ at multiple other traits as well. Studies using enzyme loci (allozymes), and DNA markers like mtDNA, microsatellites, or nuclear DNA sequences, have shown that races that form hybrid zones usually differ at one or many of these molecular markers as well.
Perhaps the record for character differences
across a hybrid zone is held by the European fire-bellied toad, Bombina
(not native to Britain, but now common as a escaped pet in parts of London).
There are two forms, Bombina bombina and B. variegata which
meet in a narrow east-west hybrid zone stretching over a large part of
Bombina bombina Bombina variegata
Habitat Lowland Hilly
Water bodies Large ponds, lakes Small ponds, puddles
Skin thickness Thin Thick
Eggs (spawn) Small, many Large, fewer
Belly warning colour Yellow Red
Other differences Male mating call
Hybrids develop less successfully
Multiple allozyme differences
mtDNA differencesHybrid zones, then, are just places where narrow clines at multiple loci occur together. There are some cases, however, where hybrid zones for morphology or chromosomes are not associated with other differences. For example, in hybrid zones between races of the warningly coloured butterfly Heliconius [SHOW OVERHEAD], there are no differences in allozymes, chromosomes, or DNA, and hybrids are apparently as fertile and viable as the normal pure forms on either side of the zone. In Heliconius, the colour pattern differences are known be inherited at a handful of major gene loci that affect warning colour alone. However, these hybrid zones may still be narrow, since selection against rare phenotypes may be as high as s 0.5. I have found that butterflies bearing rare colour patterns may have 50% of the chance of survival enjoyed by common phenotypes.
Conclusions: importance of space and time evolution
There are many definitions of species, but fundamentally, species differ genetically at multiple loci. If two species occur together in space, this divergence is maintained, and to understand their speciation, we need to know about the events that took place in a past time. Yet for most genetic studies, we only have the present; a thin film on the surface of time.
Yet because dispersal is typically limited, spatial genetic differences often give some idea of temporal patterns of divergence. In evolution, as in physics, space and time are strongly related. We can investigate intermediates on the road to speciation by examining spatial variation in natural populations.
The theory of spatial evolution and cline theory is important for understanding the limits to environmental adaptation. In some cases, migration will swamp adaptations to a particular area. But wherever the cline width, w, is substantially smaller than the environmental patches, there will be no problem for adaptation; adaptation can occur in parapatry, in spite of continued gene flow.
For the same reasons, cline theory also shows how genes for intrinsic selection will evolve spatially -- that is, very similarly to genes for environmental adaptation. The patchy structure of chromosomal races, mating types, and other kinds of genetic architectures under intrinsic selection can be almost as fine-grained as the spatial evolution genes for environmental adaptation.
Also, because hybrid zones consist of multiple clines, cline theory enables us to understand the widespread phenomenon of hybrid zones which separate taxa that are clearly on the road to speciation.
Hybrid zones separate forms, that, like
species, usually differ at many genes. Therefore the study of hybrid zones
give us a glimpse of an intermediate stage of evolution between simple
intraspecific polymorphisms and "good" species. Unlike "good" species,
hybridizing forms can be crossed, and we can therefore study the genes
that lead to incipient speciation.
FUTUYMA, DJ 1998. Evolutionary Biology. Geographic variation and clines: chapter 9 (pp. 257-262). Cline theory: chapter 13 (pp. 381-383). Hybrid zones: chapter 15 (pp. 454-456, 464-468).