Perspective conservation genetics enters the genomics era

Throughout most of my professional career (which began in the late 1960s), a long-sought Holy Grail in molecular ecology and evolution was to obtain extensive nucleic acid sequences from large numbers of loci and organisms. In lieu of efficient DNA-sequencing technologies, researchers adopted a succession of less direct approaches for estimating various genomic parameters such as heterozygosities, kinship coefficients, or genetic distances. These laboratory techniques included allozyme electrophoresis (mid-1960s), the immunological approach of micro-complement fixation (1960s), gel-sieving and other methods to reveal hidden protein variation (early 1970s), restriction-enzyme assays especially of mitochondrial DNA (late 1970s), DNA/DNA hybridization (1970s), DNA fingerprinting by minisatellites (1980s), PCR-based sequencing of particular target genes for which conservative primers were developed (late 1980s), RAPD (randomly amplified polymorphic DNA) assays (1990s), microsatellite analyses (1990s), DNA barcoding based on a mitochondrial gene (2000s), and several other molecular approaches for revealing genetic variation in particular proteins or classes of nucleic acids (see Hillis et al. 1996; Avise 2004; Freeland 2005). Different laboratory methods yielded genetic markers well-suited for addressing different sections along a phylogenetic spectrum from the microto the macro-evolutionary: detection of clonal identity or non-identity (e.g., via DNA fingerprinting or multi-locus allozymes), population demography and mating systems (allozymes, microsatellites), intraspecific population structure and phylogeography (allozymes, mtDNA), speciational processes and species differences (barcoding, allozymes, mtDNA), hybridization and introgression (allozymes, mtDNA), and supra-specific phylogenetics at many temporal scales (via microcomplement fixation, DNA-DNA hybridization, and DNA sequencing of particular nuclear or cytoplasmic loci). In many cases, the data also served to improve our mechanistic understanding of a wide range of molecular-level phenomena such as mutation rates and patterns, gene duplications, the phenomenon of concerted evolution, and the operation of natural selection on particular loci. The primary limitation of most methods (with the possible exception of DNA hybridization) was that only a tiny fraction of the genome was accessible from which to make estimates of the genome-wide parameters that ultimately were of interest. In recent years, later-generation molecular technologies have made mass-scale nucleic acid sequencing almost routine. For example, by the spring of 2009, at least one entire genome had been sequenced from each of about 1,000 species (including 100 eukaryotes), with another 1,000 species in various stages of sequence completion. Modern molecular methods such as 454 pyrosequencing also make it possible to sequence thousands of proteincoding genes using expressed sequence tags (ESTs) from the transcriptomes (messenger RNA pools) of multiple individuals, even in non-model organisms (Papanicolaou et al. 2005; Hudson 2007). Furthermore, in this ‘‘genomics revolution,’’ dramatic advancements in microchip arrays and related technologies have made gene-expression profiling (transcriptomics, proteomics, and metabolomics) practicable at unprecedented genomic scales (Gibson and Muse 2009). Indeed, molecular technologies are no longer the limiting factor in genetic analysis, often having been J. C. Avise (&) Department of Ecology and Evolutionary Biology, University of California, Irvine, Irvine, CA 92697, USA e-mail: javise@uci.edu