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Molecular Ecology (2003) 12, 1109 –1112 PREFACE TO THE SPECIAL ISSUE Blackwell Publishing Ltd. Merging Ecology, Molecular Evolution, and Functional Genetics M I C H A E L P U R U G G A N A N and G R E G G I B S O N Department of Genetics, North Carolina State University, Gardner Hall, Raleigh, NC 27695–7614, USA ‘This structure has novel features which are of considerable biological interest.’ This has to be one of the boldest understatements in all of biology, written 50 years ago in Nature by Francis Crick and Jim Watson in describing their model for the DNA double helix (Watson & Crick 1953). The unveiling of the structure of the molecule that carries the hereditary information of living organisms is rightly hailed as a landmark in the history of science, and we rightly celebrate the golden anniversary of this discovery this year. Understanding the molecular basis of genes has transformed biological research since 1953, and ecologists have participated in the fruits of this revolution. The use of molecular markers, beginning with restriction fragment length polymorphisms (RFLPs) to today’s single nucleotide polymorphisms (SNPs), has had a significant impact on our ability to trace parentage and kinship, to measure gene flow and migration patterns and to reconstruct the demographic histories of populations and species. Few will argue that the advent of modern genetic technology has provided an unparalleled ability to examine evolutionary and ecological forces in nature. Yet the full impact of molecular genetics (and today, genomics) has yet to be felt by the discipline of ecology. While the use of molecular markers by ecologists has been fruitful, there is more to the molecules than their current dominant role in ecological research as mere genetic barcodes. We have yet to understand ecological processes at a fundamentally molecular level, and our inability to make this connection from the ecological gene to the ecological organism hampers any dreams we may harbour of creating a unified picture of life. We do not know, to a large extent, the interplay between genes and the ecological processes that dominate life at and above the organismal level. We stand today at a crossroads that provide unprecedented opportunity to make these connections. Molecular biologists have proved adept at unravelling the molecular mechanisms behind many of the physiological, developmental and at times behavioural processes that characterize organismal lives. It is time that ecologists make use Correspondence: G. Gibson. Fax: (919) 515-3355; E-mail: [email protected] © 2003 Blackwell Publishing Ltd of this information in meaningful ways to gain further insights into the nature of organismal ecologies. How do we go about doing this? There is no one single answer to this question. There remains no single coherent program of molecular ecology. But it is the diversity of approaches that make this an interesting enterprise, and in this issue we try to highlight some distinct ways in which research into the nature of genes and ecology can be tackled. The papers brought together in this issue represent three complementary approaches to the molecular genetic dissection of microevolution: i) ecological genetics; ii) molecular evolutionary genetics; and iii) association studies. Ecological genetics refers to experimental manipulation of the environment for a series of genotypes representing both natural variation and carefully chosen mutations that interfere with the biological process of interest. It brings the long tradition of developmental and biochemical genetics into the realm of ecology, illustrating important ways that these all to disparate disciplines can reinforce one another. Molecular evolutionary genetics has also been in the ascendant, but there is a new push to interpret patterns of nucleotide changes (either within or between species) in the context of ecological and genomic variables, from geography to polyploidy, and to relate these patterns to diverse gene ontologies. The term ‘association study’ is used here as a catch-all phrase for the attempt to map genotype onto phenotype. It includes quantitative trait locus (QTL) mapping with and without regard to the nature of any candidate genes in QTL intervals, as well as the morenarrowly defined approach of associating segregating variation in specific genes with morphological variation within and between populations of a species. The latter is now the centrepiece of human disease genetics, but has yet to see broad application in microevolutionary analysis. If we place the three approaches on the vertices of a triangle as suggested in Fig. 1, it becomes apparent that the intellectual overlap between them is mediated by another triad of common links. Biogeographical variables such as altitude and salt stress provoke the physiological and behavioural adaptations that geneticists seek to explain, while their presence is presumed to leave a hidden signature in patterns of nucleotide variation. Genetic dissection and QTL mapping suggest candidate genes, whose identification — oftentimes borrowing from other systems — in 1110 M I C H A E L P U R U G G A N A N and G R E G G I B S O N Fig. 1 A schematic overview of the three approaches to genes and ecology described in the text, and the types of data that link them. In the coming years, various ‘omics’ (genomics, proteomics, metabolomics, for example) will feed into the approaches in a wide variety of ways. turn provides new insight into regulation and physiology. SNPs are single nucleotide or other simple polymorphisms, most of which have no functional consequence, yet nevertheless report the myriad evolutionary processes that shape the distribution of molecular variation. A major challenge for the coming decades lies in the mapping of SNP onto QTL effects, and while this seems feasible where a single change accounts for 10% of the phenotypic variation, there is still debate as to whether more subtle contributions can be detected. Missing from this collection of papers is any explicit effort to use ‘omics’ in ecological genetics. Nevertheless, it is clear that genome, transcriptome, proteome, and metabolome profiling will play an increasingly central role in feeding each of the research strategies represented here. Animals, plants, and microbes are all represented in this volume, and each of the research strategies finds application in each of the kingdoms. Perhaps the strongest demonstration of the potential for ecological genetic strategies to illuminate fundamental physiological processes comes from the plant side. Coberly & Rausher (2003) show how greenhouse studies can be used to demonstrate a novel pleiotropic function for a central biochemical pathway, namely a contribution of flavonoids to the protection of gametogenesis against heat stress. In doing so the authors provide a plausible explanation for the failure of the a floral pigmentation locus to attain high frequencies in natural populations of Ipomoea, while a similar mutation in the w locus is a common variant. Similarly, Traw et al. (2003) use genetic crosses to investigate the crosstalk between salicylate and jasmonate-mediated defense pathways in response to herbivore and bacterial pathogen exposure. Notions of antagonistic pleiotropy and trade-offs can now be studied at the level of gene expression and function, but only if genetic background and environment are controlled carefully. McKay et al. (2003) continue this theme in their comparison of mutational and segregating variance for drought resistance through physiological avoidance of dehydration and escape from drought by early flowering. They demonstrate how genotype–by–environment interactions are likely to affect the maintenance and spread of variation in field populations, and this point is taken up by Weinig et al.′s (2003) mapping of QTL for resistance to and tolerance of herbivory in Arabidopsis. They highlight significant seasonal effects on the detection of QTL, implying that ecologists should be willing to move back and forth between laboratory and field, recognizing that quantitative genetic analyses in these settings can have different power and advantages in relation to a range of research questions. On the animal side, Williams et al. (2003) describe some laboratory experiments designed to mimic the effect of rapid temperature fluctuation in the wild on wing abnormalities in fruitflies, and show that rather than being protective, HSP70 may under some circumstances sensitize the organism to stress-induced damage. Presumably organisms must balance steady-state signalling intensity against the possible benefits of protection upon induction of chaperone proteins. Even such an apparently stark physiological system as the heat shock response holds surprises when ecology is integrated with genetics. Dixon et al. (2003) take a more traditional, experimental approach in surveying phenotypic variation for sperm precedence among allopatric populations in two different species of Drosophila. While studies of a variety of animal species have demonstrated that sperm precedence often evolves more rapidly than premating isolation between species, this study of conspecifics demonstrates that this need not be the case between races. Genetic association studies have the goal of confirming that the genes that are thought to matter, really do matter. These candidate genes can arise from a variety of approaches: fine scale recombination mapping; microarray analyses; knowledge of development and physiology; and comparative genomics spring readily to mind. The conceptually most direct association strategy is to ask whether a particular allele or haplotype is significantly more prevalent in one phenotypic class than another. This is clearly the case for a haplotype of the melanocortin receptor Mcr1 that distinguishes two melanic classes of rock pocket mice in Arizona studied by Hoekstra and Nachman (2003). They show though, that similar cases of adaptive colouration in New Mexico populations must involve different loci, providing one of the first instances of genetic heterogeneity for convergent evolution. Not all candidate loci, however, show an association as predicted by both molecular genetic and ecological studies. Garcia-Gil et al. (2003), in a study of nucleotide polymorphism in the phytochrome © 2003 Blackwell Publishing Ltd, Molecular Ecology, 12, 1109 –1112 M E R G I N G E C O L O G Y , M O L E C U L A R E V O L U T I O N , A N D F U N C T I O N A L G E N E T I C S 1111 genes in Pinus sylvestris, show very low levels of variation that are not correlated with timing of budset in this forest conifer. What is surprising is the very low level of nucleotide variation in this species for these and other genes. The associations that are observed need not necessarily be direct, but may hint at population structuring that underlies phenotypic differences. Along these lines, McGovern and Hellberg (2003) report a very interesting association in northern vs. southern populations of the bryozoan Bugula neritina. In this species, larvae from southern populations produce chemical deterrents to fish predators that northern populations lack. Using COII mitochondrial markers, they show population differentiation between northern and southern B. neritina populations. Moreover, RNA markers indicate that only the southern populations have an association with the γ-proteobacteria E. sertula, which produces bryostatins that may act as the fish deterrents. This study nicely illustrates the use of molecular markers to identify bacterial associations that confer phenotypic advantages to host species. Most complex traits are likely to be influenced by many genes, and given the expense of genotyping the hundreds of individuals required for statistical power, a first analytical step will often be the establishment of linkage in controlled crosses between morphologically divergent parents. Voss et al. (2003) achieve this for one of two thyroid hormone receptors that they sampled in Ambystomatid salamanders in relation to metamorphic timing. They also find strong genetic background effects, suggesting that both the magnitude and direction of effects will be particular to divergent lineages. Lexer et al. (2003) provide a more complicated application of QTL mapping technology in simultaneously detecting quantitative determinants of mineral ion uptake and survivorship in a salt-tolerant species of hybrid sunflowers, Helianthus paradoxus. They argue that transgressive segregation facilitated rapid exploration of a new ecological niche, namely a salt marsh, as a result of selection for recombinant lines with favourable patterns of complementary alleles affecting calcium uptake and sodium exclusion. A very different type of candidate gene study is presented by Miller (2003), who used maximum likelihood methods to identify amino acid variants in the rbcL gene of a clade of hot spring cyanobacteria that may have been selected for thermotolerance. The author then located the residues on the tertiary structure of the protein, suggesting specific hypotheses for the molecular basis of thermotolerance that can now be addressed in the laboratory. The sequence surveys presented in this special issue also cover numerous topics with varying linkage to proximate ecological causes. In a study comparing genes from the selfing A. thaliana to the outcrossing A. lyrata, Wright et al. (2003) explores the effect of mating system on levels of © 2003 Blackwell Publishing Ltd, Molecular Ecology, 12, 1109–1112 molecular variation, which can have implications for the dynamics of selection as well as strategies for candidate association studies in these species. A more explicit discussion of the effect of environmental agents on the distribution of allelic variation comes from Watt et al.′s (2003) ongoing study of Pgi polymorphism in Colias species. They contrast the uniformity of allozyme frequencies in lowland butterflies throughout Western North America with a sharp discontinuity associated with altitude (but not geographical distance) in the alpine species, C. meadii. Duvernell et al. (2003) also consider geography in their survey of clinal variation associated with the methuselah locus in D. melanogaster, but with the twist that they are able to demonstrate that two tandem duplicate paralogs experience different selection pressures: only the more variable gene shows the clinal distribution. They also argue that between 2% and 10% of all fly genes may be subject to geographically structured selection, challenging the notion of panmixia in this cosmopolitan species. In another study of tandem duplicates, the defense-related trypsin inhibitor ATTI loci of Arabidopsis, Clauss and Mitchell-Olds (2003) show how life history can strongly impact molecular evolution, in so far as evidence for differential selection pressure is only seen in the outcrossing species A. lyrata and not in the heavily inbreeding A. thaliana. They also make a case for subfunctionalization of trypsin inhibitor protein domains on the basis of complementary patterns of amino acid divergence. Lawton-Rauh et al. (2003) add a further level of complexity in their consideration of the effect of allopolyploidy on divergence of doubly paralogous copies of two floral homeotic gene families in the Hawaiian silversword alliance. Their conclusion is that duplicate copies do experience different evolutionary trajectories, but that single genes must be considered in the genomic context of levels of duplication. By contrast, Riley et al. (2003) focus on a cassette of single-copy genes involved in Ras-mediated signal transduction in Drosophila. They show that constraint is highest for genes at the top of the biochemical pathway and suggest that the molecular ecology of these genes should be understood in light of biophysical models of intracellular signalling — much as metabolic control theory has been invoked to explain patterns of balancing selection in enzyme pathways. Jovelin et al. (2003) add behavioural ecology to the picture by developing chemosensation in the soil nematode Caenorhabditis as a model quantitative genetic study system. Much like the Wright et al. study in Arabidopsis species, mating system is seen to be a major factor here as well; the outbreeding species C. remanei shows more variation in the odr3 gene than does self-fertilizing C. elegans. One point that is clear from all of these surveys is that different classes of gene experience very different selection pressures. This is perhaps not surprising, but the point is 1112 M I C H A E L P U R U G G A N A N and G R E G G I B S O N that despite two decades of molecular population genetics, we are little closer to a general theory of the relationship between genetic variation and phenotypic variation than were the architects of the modern synthesis. As genomics opens up, more and more opportunities for testing, not just single genes, but whole complexes of genes, data will accumulate with the potential for quite profound shifts in understanding. However, knowledge will only accrue when data is analysed and generated with increasingly sophisticated experimental designs that incorporate physiology and ecology into evolutionary genetics along the lines hinted at in this issue. References Clauss MJ, Mitchell-Olds T (2003) Population genetics of tandem trypsin inhibitor genes in Arabidopsis species with contrasting ecology and life history. Molecular Ecology. Coberly LC, Rausher MD (2003) Analysis of a chalcone synthase variant in Ipomoea purpurea. Reveals a Novel Function for the flavonoids: ameliorating heat stress. Molecular Ecology. Dixon SM, Coyne JA, Noor MAF (2003) The evolution of conspecific sperm precedence in Drosophila. Molecular Ecology. Duvernell DD, Schmidt PS, Eanes WF (2003) Clines and adaptive evolution in the methuselah gene region in Drosophila melanogaster. Molecular Ecology. Garcia-Gil MR, Mikkonen M, Savolainen O (2003) Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Molecular Ecology. Hoekstra HE, Nachman MW (2003) Different genes underlie adaptive melanism in different populations of rock pocket mice. Molecular Ecology. Jovelin R, Ajie BC, Phillips PC (2003) Molecular evolution and quantitative variation for chemosensory behavior in caenorhabditid nematodes. Molecular Ecology. Lawton-Rauh A, Robichaux RH, Purugganan MD (2003) Patterns of nucleotide variation in homeologous regulatory genes in the allotetraploid Hawaiian silversword alliance (Asteraceae). Molecular Ecology. Lexer C, Welch ME, Durphy JL, Rieseberg LH (2003) Natural selection for salt tolerance QTL in wild sunflower hybrids: Implications for the origins of Helianthus paradoxus, a diploid hybrid species. Molecular Ecology. McGovern TM, Hellberg ME (2003) Cryptic species, cryptic endosymbionts and geographic variation in chemical defense in the bryozoan Bugula neritina. Molecular Ecology. McKay JK, Richards JH, Mitchell-Olds T (2003) Genetics of drought adaptation in Arapidopsis thaliana. I. Pleiotropy contributes to genetic correlations among ecological traits. Molecular Ecology. Miller SR (2003) Evidence for the adaptive evolution of the carbon fixation gene rbcL during diversification in thermotolerance of a clade of hot spring cyanobacteria. Molecular Ecology. Riley RM, Jin W, Gibson G (2003) Contrasting selection pressures on components of the Ras-mediated signal transduction pathway in Drosophila. Molecular Ecology. Traw MB, Kim J, Enright S, Cipollini DF, Bergelson J (2003) Negative cross-talk between salicylate and jasmonate-mediated pathways in the Wassilewskija ecotype of Arabidopisis thaliana. Molecular Ecology. Voss SR, Prudic K, Oliver J, Schaffer (2003) Candidate gene analysis of metamorphic timing in ambystomatid salamanders. Molecular Ecology. Watson JD, Crick FHC (1953) A Structure for Deoxyribose Nucleic Acid. Nature, 171, 737–738. Watt WB, Wheat CW, Meyer EH, Martin J-F (2003) Adaptation at Specific Loci. VII. Natural selection, dispersal, and the diversity of molecular-functional variation patterns among butterfly species complexes. Colias: Lepidoptera, Pieridae. Molecular Ecology. Weinig C, Stinchcombe JR, Schmitt J (2003) QTL architecture of resistance and tolerance traits in Arabidopsis thaliana in natural environments. Molecular Ecology. Williams KD, Helin AB, Posluszny J, Roberts SP, Feder ME (2003) Effect of heat shock, pre-treatment, and hsp70 copy number on wing development in Drosophila melanogaster. Molecular Ecology. Wright SI, Lauga B, Charlesworth D (2003) Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Molecular Ecology. © 2003 Blackwell Publishing Ltd, Molecular Ecology, 12, 1109 –1112