Lineage sorting

The contrasting phylogenetic patterns in reproductively isolated populations in Figure 5.10 assume that the populations are genetically distinct from one another, but this is not always the case because when two populations first become isolated from one another they may both harbour copies of the same ancestral alleles. Over time, they will go through a process known as stochastic lineage sorting (Avise et al., 1983), which must occur before alleles become population-specific. Lineage sorting is driven primarily by genetic drift, and occurs when differential reproduction causes some alleles to be lost from the population simply by chance, whereas other alleles proliferate. When two populations (A and B) first diverge, and little lineage sorting has occurred, there is a high probability that these two populations will be polyphyletic. This means that because of their common ancestry some alleles in population A will be more similar to some alleles in population B than to other alleles in population A, and vice versa (Figure 5.11).

After lineage sorting has progressed for a time, populations will be paraphyletic if the alleles in population A are more closely related to one another than they are to any of the alleles in population B, but some of population B's alleles are more closely related to some of population A's alleles than they are to each other (or vice versa). After more time has elapsed both populations become monophyletic, a situation that is also known as reciprocal monophyly. When this stage has been reached, all alleles within populations are genetically more similar to each other

Polyphyly

Paraphyly

Monophyly

B7 B6 A5 B5

B4 B3 A4 A3 B2

B1 A2 A1

B7 B6 A5 B5

A4 A3

A2 A1 A6

B7 B6

LrB5

A4 A3

A2 A1 A6

Time

Figure 5.11 Progression from polyphyly to monophyly in two recently separated, reproductively isolated populations that are undergoing lineage sorting. Letters A and B refer to the populations in which the different alleles were found. After the populations are separated they are polyphyletic, because some of the alleles in population A are most closely related to some of the alleles in population B, and vice versa. Over time, alleles are both gained (following mutation) and lost (following selection or drift), leading to an intermediate stage in which population A is paraphyletic with respect to population B. Eventually the populations become monophyletic, which occurs when all A alleles are genealogically most similar to one another and all B alleles are genealogically most similar to one another than they are to the alleles that are found in other populations (Figure 5.11). It is only at this point that populations are genealogically distinct from one another.

The time that it takes for a pair of unconnected populations to reach the stage of reciprocal monophyly is directly proportional to the sizes of the populations in question. It will also depend on which genome is represented by the molecular markers that are being used. For mitochondrial and plastid DNA - which, as we know, are haploid and in most cases uniparentally inherited - time to monophyly is approximately Ne generations. In diploid species, unless there are unusual circumstances such as a biased sex ratio, time to monophyly is usually around four times longer for nuclear than mitochondrial genes because of the proportionately larger effective population size of nuclear genes (4Ne generations; Pamilo and Nei, 1988). Lineage sorting is even slower in polyploid genomes because they will have a correspondingly larger number of alleles at each locus.

The potentially confounding effects that lineage sorting has on the phylogenetic reconstructions of closely related populations or species was illustrated by a study of Solanum pimpinellifolium, a wild relative of the cultivated tomato S. lycopersicum (Caicedo and Schaal, 2004). Samples were taken from 16 populations along the northern coast of Peru and sequenced at a nuclear gene called fruit vacuolar invertase (Vac). One allele was identified as a recombinant and removed from the genealogical analyses. A maximum parsimony phylogeny was uninformative because it yielded five equally parsimonious trees, whereas a parsimony network revealed an unambiguous genealogical relationship among alleles. Perhaps the most surprising result was a lack of geographical structuring, which was unexpected because gene flow in this species is generally low and therefore some population differentiation was anticipated. The most likely explanation for these findings was the retention of ancestral polymorphism at the Vac locus, i.e. there has been insufficient time for lineage sorting to result in monophyletic (genetically distinct) populations.

Differential rates of lineage sorting provide one reason for disagreement between the nuclear and mitochondrial gene genealogies that are used in phylogeographic studies (Table 5.4). Because different genes 'sort' at different rates, the potential for discrepant genealogical relationships based on nuclear and mitochondrial genes will remain until populations have become reciprocally monophyletic with respect to all genes. Although widespread, monophyly is far from universal. A review of 584 studies compared the mitochondrial haplotype distributions of 2319 animal species (mammals, birds, reptiles, amphibians, fishes and invertebrates) and found that 23.1 per cent were either paraphyletic or polyphyletic (Funk and Omland, 2003). Other reasons for discordance between nuclear and mitochondrial phylo-geographic inferences include recombination, sex-biased dispersal and hybridization (Table 5.4). The latter is a widespread phenomenon that has often obscured the evolutionary histories of populations and species. In the following section we will therefore look in more detail at how past hybridization can influence -- and sometimes confound -- our understanding of phylogeography.

Table 5.4 Some examples showing how nuclear and mitochondrial data can generate conflicting results in phylogeographic analyses. There are a number of reasons for such discrepancies, including different dispersal patterns of males and females, introgression of some but not all genomic regions following past hybridization events, and different rates of genetic drift (lineage sorting) in nuclear and cytoplasmic genomes

Table 5.4 Some examples showing how nuclear and mitochondrial data can generate conflicting results in phylogeographic analyses. There are a number of reasons for such discrepancies, including different dispersal patterns of males and females, introgression of some but not all genomic regions following past hybridization events, and different rates of genetic drift (lineage sorting) in nuclear and cytoplasmic genomes

Mitochondrial

Nuclear

Possible

Species

phylogeography

phylogeography

explanation

Reference

Humpback

Differentiation

Hawaii and

Different rates

Palumbi and

whales

between Hawaii

California

of genetic drift

Baker

(Megaptera

and California

populations show in the two

(1994)

novaeangliae)

populations

little genetic differentiation

genomes; differential dispersal of males and females

Rainbow

Population

Populations

Differential

Bagley and

trout

differentiation

showed

introgression of

Gall (1998)

(Oncorhynchus

twice as high

relatively

mitochondrial

mykiss)

compared with

low genetic

and nuclear

that based on

differentiation.

genes following

nuclear DNA

Lack of

past hybridization

concordance

between

mitochondrial

and nuclear

phylogenies

Green turtle

Significant

Population

Male-mediated

Bowen et al.

(Chelonia

population

subdivision

gene flow;

(1992);

mydas)

subdivision on

between, but

female nest

Karl,

regional and

not within,

site philopatry

Bowen and

global scales

ocean basins

Avise (1992)

Eider duck

Substantial

Little

Male-mediated

Tiedemann

(Somateria

differentiation

differentiation

gene flow;

et al. (2004)

mollissima)

among both

among colonies;

female

local colonies

isolation by

breeding site

and distant

distance at a

philopatry

geographical

regional scale

regions

Once thought of as an anomaly, interspecific hybridization is now known to be widespread in many different taxonomic groups. We do not know how many species hybridize in nature, although the total number includes at least 23 675 species of plants (Knoblach, 1972), 3759 species offish (Schwartz, 1972, 1981), and approximately 10 per cent of bird species (Grant and Grant, 1992b). Probably even more widespread is the hybridization that occurs within species following the interbreeding of 'individuals from two populations, or groups of populations, which are distinguishable on the basis of one or more heritable characters' (Harrison, 1990). Many of the examples in this section will refer to interspecific hybridization, but while reading this you should keep in mind that much of the theory is equally applicable to hybridization between individuals from intraspecific populations.

If the two parental forms are morphologically distinct, then hybrids often can be identified from their intermediate phenotypes. Traditional breeding experiments and controlled crosses can also be valuable techniques for investigating hybridization. In wild populations, however, an increasing number of hybrids have been identified in recent years from genotypic data. As we saw in Chapter 2, this is possible because hybridization leads to the introgression of alleles across species boundaries, a process that often leads to cytonuclear disequilibrium. This introgression, combined with the preponderance of hybrids in virtually every taxonomic group, means that hybridization has become a relatively common explanation for unexpected distributions of alleles. Substantial introgression can occur even when hybridization is infrequent. Hybrids between native red deer (Cervus elaphus) and introduced Japanese sika deer (C. nippon) on the island of Argyll in Scotland were identified from mtDNA sequences and microsatellite alleles (Goodman et al., 1999). Hybridization between the two species is infrequent and therefore introgression of alleles is rare at any one locus; however, where the two species come into contact with each other, up to 40 per cent of deer carry alleles that apparently have been transferred from one species to the other.

Patterns of introgression and cytonuclear disequilibrium can be complicated further by Haldane's rule (Haldane, 1922), which states that hybrids are less likely to be viable in the heterogametic sex, i.e. the one that has two different sex chromosomes (e.g. male mammals that are XY or female birds that are ZW; Chapter 2). Evidence for Haldane's rule has been found in a number of taxonomic groups, including mammals, birds and insects. In one example, the effects of Haldane's rule on cytonuclear disequilibrium were illustrated by a study of two species of swallowtail butterflies, Papilio machaon and P. hospiton, on the islands of Sardinia and Corsica. In Lepidoptera, females are heterogametic. If, as predicted by Haldane's rule, female butterfly hybrids are unfit, mtDNA will not be transferred between species because it is transmitted maternally. On the other hand, nuclear genes may move between species via male hybrid butterflies, which are homogametic and therefore more likely to be viable. This was indeed the pattern in the two Papilio species: hybridization has resulted in the introgression of alleles at some nuclear allozyme loci but there is no evidence of mitochondrial introgression (Cianchi et al., 2003). Haldane's rule can therefore explain how nuclear introgression can occur in the absence of mitochondrial introgression.

Hybrid zones

It should be evident by now that alleles can be shared between species either as a result of shared ancestral polymorphism (incomplete lineage sorting) or hybridization (introgression of alleles), but how easy is it for researchers to differentiate between these two possibilities? This will depend on both the history and the geographical distributions of the two species. If they are recently diverged species that live entirely in sympatry, then it may be impossible to distinguish between the two scenarios solely on the basis of molecular data. In other situations, however, it may be possible to identify the source of shared alleles by looking at the distribution of these alleles across the species' geographical ranges. If two putatively hybridizing species share alleles when they are living sympatrically, but not when they are living allopatrkaUy, then hybridization is a likely explanation for these shared alleles. On the other hand, if shared alleles occur in both sympatric and allopatric populations, incomplete lineage sorting may be a more plausible explanation. Additional clues about the evolutionary histories of species may therefore be found in hybrid zones, the areas of contact in which species meet and interbreed (see also Box 5.1).

Hybrid zones are very common; some estimates suggest that they may subdivide as many as one-half to one-third of species (Hewitt, 1989). The geographical extent of these zones varies dramatically, with some that are only a few metres wide and others that span many kilometres. Hybrid zones are often linear, such as the one represented by a narrow line throughout central Europe that subdivides the two house mouse species Mus musculus and M. domesticus (Hunt and Selander, 1973). There are also mosaic hybrid zones, which are patchy in their distribution. The field crickets Gryllus pennsylvanicus and G. firmus in eastern USA interbreed throughout a well-studied mosaic hybrid zone (Harrison, 1986; Rand and Harrison, 1989). Initial studies suggested that the two species were largely allopatric, with G. firmus populations near the coast giving way to G. pennsylvanicus populations further inland, and a roughly linear hybrid zone at their juncture. This interpretation was later modified when G. pennsylvanicus populations were found within 10 km of the coast, and hybrid populations were found approximately 100 km inland. We know now that the hybrid zone between these two species is in fact a complex mosaic that spans a relatively broad geographical area.

There are two ways in which hybrid zones can be maintained. The first is based on the premise that hybrid zones are independent of their environment and are simply the by-product of two populations coming into contact with each other. Under this model, hybrids are less fit than either of the parental populations and the hybrid zone is maintained by a balance between dispersal of parental genotypes and selection against hybrids, creating a so-called tension zone (Barton and Hewitt, 1985). One example of this occurs in the zones of hybridization between the smooth-shelled marine mussels Mytilus edulis and M. galloprovincialis. Both species have a planktonic larval stage and therefore can disperse over relatively long distances. Despite this potential for frequent contact, hybridization is restricted to discrete hybrid tension zones in which the viability of hybrids, relative to either parental form, is substantially reduced at the larval stage (Bierne et al., 2002).

Hybrid zones can also be maintained in regions where hybrids have greater fitness than non-hybrids, a phenomenon that is known as bounded hybrid superiority (Moore, 1977). When hybrids are favoured under certain conditions, parental forms and hybrids will often be distributed along an environmental gradient that alternately favours either form. One example of this was found in a study that used AFLP markers to compare the genotypes of four hybridizing western North American oak species (Quercus wislizenii, Q. parvula, Q. agrifolia and Q. kelloggii) with climatic variables to see if there were particular conditions that seemed to favour hybrids (Dodd and Afzal-Rafii, 2004). Hybridization between these species is not restricted to bounded hybrid zones, in part because pollen dispersal can lead to allopatric hybridization. In the Quercus study, hybrids were sometimes separated by at least 300 km from one of the parental species, suggesting a mosaic hybrid structure across a broad spatial scale. Parental and hybrid forms were each associated with a particular set of environmental variables, including temperature, precipitation, vapour pressure deficits and solar radiation. These associations imply that 'pure' species and hybrids are being selected for under different environmental conditions.

Box 5.1 Hybridization and speciation

One reason why hybrid zones have been the focus of so many studies over the past few decades is that they provide fascinating arenas of evolution and, in some cases, speciation. Reticulated evolution occurs when hybridization results in the formation of new species. This may occur either within hybrid zones or following seemingly random hybridization events. Recall from Chapter 3 that hybridization can lead to speciation through the creation of genetic diversity (see Box 3.5). A simpler mechanism of hybrid speciation occurs when two parental species interbreed and a new species results. This may or may not entail an increase in ploidy (Figure 5.12). In plants, polyploidy is extremely common; in fact, the frequency of allopolyploidy (Chapter 1) has been interpreted as evidence that the majority of plant species are either of direct hybrid origin or descended from a hybrid species (Grant, 1981). Less commonly, new species arise following homoploid hybrid speciation, which occurs when the hybrid has the same ploidy as its parental species. An example of this has been found in Iris nelsonii, which, according to data from allozymes, cpDNA and RAPDs, was derived from hybridization between three species (I. fulva, I. hexagona and I. brevicaulis) (Arnold, 1993).

In vertebrates, bisexual allopolyploid hybrid species are not uncommon in fishes and frogs. In addition, virtually all of the 70 unisexual vertebrate taxa that have been identified so far, which include species of fish, lizards and salamanders, arose following the hybridization of parental forms. More recently, hybrid speciation has been documented in marine invertebrates. Within the soft coral genus Alcyonium, A. hibernicum contains two groups of closely related sequences from the nuclear ribosomal internal transcribed spacer (ITS) region. One of these groups matched sequences that were also found in A. coralloides, whereas sequences in the other group matched those found in an, as yet, undescribed species that is currently designated A. sp. M2 (McFadden and Hutchinson, 2004). The most likely explanation for this pattern is that A. hibernicum arose following hybridization between A. coralloides and A. sp. M2. The conclusion that this species has a hybrid origin is further supported by its mode of reproduction, which is either parthenogenesis or obligate selfing, two mechanisms that are common to other well-studied uni-sexuals of hybrid origin.

Helianthus annuusX Helianthus petiolaris 2n (diploid) 2n (diploid)

Helianthus anomalus 2n (diploid)

Erythronium montanum X Erythronium revolutium 2n (diploid) 2n (diploid)

Erythronium quinaultense 4n (tetraploid)

Figure 5.12 Hybrid speciation in plants. (A) Homoploid speciation - in this case in sunflowers -occurs when the newly formed species has the same ploidy level as its progenitors (Rieseberg et a/., 1993). (B) Polyploid speciation in lilies occurred when two hybridizing diploid species gave rise to a tetraploid species (Allen, 2001)

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