Uniparental markers a cautionary note

Although uniparental markers have many useful applications in molecular ecology, it is important to keep in mind that they also have some drawbacks. We have referred already to the high recombination rates of plant mtDNA and the low mutation rates of cpDNA, and whereas neither of these considerations is particularly relevant to animal mtDNA, there are other limitations that are common to all mtDNA and cpDNA markers. For one thing, organelles behave as single inherited units and are therefore effectively single locus markers. As we will see throughout this text, data from a single locus allow us to retrace the history of only a single genetic unit (gene or genome), which may or may not be concordant with the history of the species in question. This is particularly true of mtDNA, cpDNA and Y chromosomes because their reduced effective population sizes, relative to autosomal DNA, mean that their haplotypes have a greater probability of going extinct. This loss of haplotypes can cause researchers to infer an oversimplified population history or to underestimate levels of genetic diversity.

An additional drawback to uniparentally inherited markers is that they may not be representative of populations as a whole. We have seen already how the inheritance of markers can influence our understanding of the dispersal patterns of plants depending on whether we target mtDNA, cpDNA or nuclear genomes. The same can be true in animals if dispersal is undertaken by only one gender, e.g. if males disperse and females do not, the mtDNA haplotypes would be population-specific and mtDNA data may lead us to conclude erroneously that individuals never move between populations.

Another risk associated with mtDNA markers involves copies of mtDNA that have been translocated to the nuclear genome; these are known as mitochondrial pseudogenes, or numts (nuclear copies of mtDNA sequences). Once they have been transposed into the nucleus, these non-functional pseudogenes continue to evolve independently of mtDNA. Problems will arise from this during PCR if the primer-binding sites have been conserved in the pseudogene, which then may be amplified in addition to, or instead of, the desired mitochondrial region. Although not evenly distributed across taxa, nuclear copies of mitochondrial DNA have been found in more than 80 eukaryotic species, including fungi, plants, invertebrates and vertebrates (reviewed in Bensasson et al., 2001). Steps can be taken that often greatly reduce the likelihood of amplifying these mitochondrial pseudogenes, although one study that specifically set out to investigate this problem concluded that the high frequency of numts in gorillas, combined with their overall similarity to true mtDNA sequences, meant that the application of mtDNA analysis in this species should be undertaken only with extreme caution (Thalman et al., 2004).

A final note about uniparentally inherited markers is that their applications are somewhat different in asexually reproducing organisms. Up to this point our discussion has centred, either implicitly or explicitly, on sexually reproducing organisms, but of course not all organisms reproduce in this way. A large proportion of prokaryotes, plus numerous eukaryotes (plants, invertebrates and some vertebrates), can reproduce asexually (Table 2.3). In the absence of sex, there is no distinction between genomes that are uniparentally and biparentally inherited. Note, however, that the picture is often complicated by the fact that many species are capable of both sexual and asexual reproduction. For example, reproduction of the grain aphid (Sitobion avenae) appears, for the most part, to be predominantly asexual in the north and sexual in the south of Britain, although

Table 2.3 Some methods of asexual reproduction

Method of reproduction Examples

Vegetative reproduction (asexual reproduction from somatic cells).

Includes:

• Budding. An offspring grows out of the body of the parent

• Fragmentation. Body of parent breaks into distinct pieces, each of which can form offspring

• Rhizomes and stolons. Runners that give rise to new individuals

• Regeneration. If a piece of a parent is detached, it can grow and develop into a new individual

Parthenogenesis (asexual reproduction via eggs). Includes:

• Apomixis (mitotic parthenogenesis). The development of an individual from an egg that has not been fertilized, and which has a full complement of the mother's chromosomes. Because there is no involvement of a male gamete, it leads to the production of offspring that are genetically identical to the mother

• Amphimixis (meiotic parthenogenesis). Female parent produces eggs by meiosis, which develop without uniting with a male gamete. The diploid state is restored either by a cell division that doubles the number of chromosomes or by fusion of the egg nucleus with another maternal nucleus

Hydra, planarians Opuntia cactus

Strawberries Echinoderms

Aphids, dandelions, flatworms, water fleas, rotifers, whiptail lizards Bagworm moth Solenobia; nematodes (genus Heterodera)

this seems to depend partly on the climate (Llewellyn et al., 2003). Research into the population genetics of species that have multiple reproductive modes often requires more data than can be obtained from a uniparentally inherited marker.

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