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Efficient Genetic Markers for Population Biology Paul Sunnucks

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Efficient Genetic Markers for Population Biology Paul Sunnucks REVIEWS Efficient genetic markers for population biology Paul Sunnucks n the past decade, several key Population genetics has come of age. Three laboratory (or, indeed, just to col- advances in molecular genetics important components have come together: laborate with a convenient lab- Ihave greatly increased the im- efficient techniques to examine informative oratory), rather than choosing pact of population genetics on segments of DNA, statistics to analyse DNA the suite of genetic markers that biology. Most important have data and the availability of easy-to-use would best answer the question been: (1) the development of computer packages. Single-locus genetic and then obtaining those data. polymerase chain reaction (PCR), markers and those that produce gene We might consider three levels of which amplifies specified stretches genealogies yield information that is truly molecular change that would pro- of DNA to useable concentrations; comparable among studies. These markers vide information at different lev- (2) the application of evolution- answer biological questions most efficiently els of population biology (Box 1). arily conserved sets of PCR primers and also contribute to much broader First, the most sensitive genetic (e.g. Ref. 1); (3) the advent of investigations of evolutionary, population and signals are genotypic arrays, most hypervariable microsatellite loci2,3; conservation biology. For these reasons, commonly encountered in the and (4) the advent of routine DNA single-locus and genealogical markers should form of multiple microsatellite sequencing in biology laborator- be the focus of the intensive genetic data loci scored in samples of individ- ies. These innovations, coupled collection that has begun owing to the power uals. In sexual species, these with the recent explosion of power- of genetics in population biology. arrays are reshuffled at each gener- ful analyses and relatively user- ation, and, therefore, are useful friendly computer programs4,have for the shortest- and finest-scale meant that much of the power Paul Sunnucks is at the Dept of Biological Sciences, population processes, such as inherent in molecular genetic data Monash University, VIC 3168, Australia individual identification and track- ([email protected]). can be tapped, revealing otherwise ing, parentage and relatedness of unobtainable information at all interacting individuals9–12. How- levels of biotic hierarchy3,5–7. The ever, arrays can be recognizable profound contribution of molec- for longer in organisms without ular genetics is reflected in Molecular Ecology being among frequent genetic recombination13. Second, microsatellites, the most cited primary ecological and/or evolutionary mitochondrial DNA (mtDNA) and other single-locus mark- journals (Institute for Scientific Information). ers (definitions and details in Boxes 2 and 3) can also be analysed as individual genes with frequencies and geo- ‘Natural history of DNA’ results in a trail graphic distributions (genic analyses). These properties of information change on larger spatial and temporal scales than geno- Individual organisms differ in the DNA sequences compris- typic arrays, and are effective markers of gene flow and ing their genomes. This genetic variation can be considered population history, even in species with limited genetic at the level of individual genes (genic) or of genotypes variation14,15. Third, slower again is the creation of new (genotypic). The fate of a given genetic variant in time and alleles by mutation, thus the analysis of their evolutionary in space will be influenced by the biology and circum- relationships (allele and/or gene genealogies, or phy- stances of the individuals through which it passes, includ- logenies) is informative about the longer-term processes ing reproductive success, migration, population size, nat- of phylogeography, speciation and deeper taxonomic ural selection and historical events. Population genetic phylogenetic reconstruction8. models investigate the connection between these demo- graphic features and the distribution of molecular genetic Basic properties of genetic markers in variants7,8. By measuring genetic variation and by applying population biology population genetic models, we can make inferences about There is an apparently bewildering array of genetic tech- the biology of organisms. Processes that affect individuals niques available for population genetic analysis5,7,16. How- ultimately accumulate into effects on populations, which, in ever, ignoring technical details and focusing on important turn, influence speciation, and so on up the taxonomic hier- properties helps to make sense of the methods. Genetic archy8. Thus, by examining genetic markers with appropri- markers are simply heritable characters with multiple ate rates of change, and, therefore, suitable signals, infor- states at each character. Typically, in a diploid organism, mation can be obtained about almost any population and each individual can have one or two different states evolutionary process through the hierarchy of life. (alleles) per character (locus). All genetic markers reflect The rates of change of the distributions of different differences in DNA sequences, usually with a trade-off genetic markers vary owing to the differential action of between precision and convenience. Separate loci can pro- fundamental processes, including recombination, mutation vide independent tests of hypotheses, thus using many and selective constraint (Box 1). Selecting appropriate together can yield extreme sensitivity. Genetic variation genetic analysis is vital to the success of applying molecu- is usually organized hierarchically (for example, two al- lar genetics in population biology. It is a surprisingly com- leles within an individual, N individuals within a subpopu- mon mistake just to use techniques that are available in a lation and Y subpopulations within populations). Thus, data TREE vol. 15, no. 5 May 2000 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(00)01825-5 199 REVIEWS Recent major advances in analysis in molecular Box 1. Rates of change of the major categories of genetic population biology variants in population biology After some considerable lags behind theory (mostly be- Genotypic cause suitable data were not readily available before the Genotypic arrays (composite genotypes of multiple loci): individual geno- advent of microsatellites), population genetic analysis is types are labile – a single round of sexual recombination usually destroys a making great use of maximum likelihood, Bayesian statis- genotype. They are quantified most rigorously using multiple single-locus tics and Markov chain Monte Carlo simulation techniques nuclear markers (typically microsatellites) (see Boxes 2–4 and Table 1 for 4,17,18 definitions concerning, and attributes of, genetic markers). to extract more information from genetic data . A fun- • Application: the individual level, including movements of individuals, non- damental advance is the development of analyses of gene invasive sampling, parentage and relatedness of interacting individ- genealogies focusing on evolutionary relationships among uals7,9,11,12,17,28. Attributes of individual genotypes can address questions individual alleles sampled from populations within such as the relationship between inbreeding and/or outbreeding and fitness4. species3,19 (Box 4). These techniques (notably ‘coalescence Interlocus allelic correlations (linkage disequilibrium, LD): associations of al- approaches’3,4,8,19 and ‘nested clade analysis’19) allow clear leles at pairs of nuclear loci will persist according to their recombination rate, testing of historical and spatial hypotheses, such as distin- the effective population size (Ne) and natural selection. Textbook population genetics holds that newly generated correlations of unlinked loci in ideal guishing current restricted gene flow from past gene flow, populations decay to zero in approximately ten generations, but associations and investigating the direction and relative timing of among linked loci might persist for hundreds or thousands of generations. events, such as range expansions. Finally, models of molecu- • Application: population level including Ne estimation, understanding lar evolutionary change are becoming sophisticated and metapopulation dynamics, and recognizing recent colonizations and intro- can greatly improve genealogical inference16. These devel- ductions7,29. opments have resulted in fundamental advances in what Genic can be learnt about populations. Luikart and England4 cite Allele and/or haplotype frequencies are population statistics that can be changed by genetic drift, founder effect, gene flow and selection. They are 26 different analyses in four categories of population biol- estimated most accurately from multiple, separate, nuclear loci and mito- ogy [relatedness and parentage, dispersal and migration, chondrial DNA (mtDNA). inbreeding, and effective population size (Ne )] that can pro- • Application: includes estimating gene flow and population subdivision8. vide previously unattainable information, and this counts Gene genealogies only those primarily involving microsatellites. The new Sequence of mtDNA or nuclear genetic regions [microsatellites and single approaches are making great strides in analysing nonequi- copy nuclear (scn) markers] will evolve as determined by the mutation rate, librium situations that predominate in conservation biology
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