Evolution of Genome–Phenome Diversity Under Environmental Stress
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Evolution of genome–phenome diversity under environmental stress Eviatar Nevo* Institute of Evolution, University of Haifa, Haifa 31905, Israel This contribution is part of the special series of Inaugural Articles by members of the National Academy of Sciences elected on May 2, 2000. Contributed by Eviatar Nevo, March 5, 2001 The genomic era revolutionized evolutionary biology. The enigma diploids, inbreeders and outbreeders, as well as sedentary and of genotypic-phenotypic diversity and biodiversity evolution of migratory organisms. Our ecological theaters include global (the genes, genomes, phenomes, and biomes, reviewed here, was entire planet), regional (Israel and the Near East Fertile Cres- central in the research program of the Institute of Evolution, cent), and local (several microsites in the Galilee Mountains University of Haifa, since 1975. We explored the following ques- Neve-Yaar, Yehudiyya, Tabigha, and Ammiad) studies, and the tions. (i) How much of the genomic and phenomic diversity in model system in the Carmel and Galilee Mountains. nature is adaptive and processed by natural selection? (ii) What is The environmental stresses analyzed include thermal, chem- the origin and evolution of adaptation and speciation processes ical, climatic, and biotic, studied in the field and under critical under spatiotemporal variables and stressful macrogeographic and laboratory conditions. The biological systems include pheno- microgeographic environments? We advanced ecological genetics types (morphological, physiological, and behavioral) and geno- into ecological genomics and analyzed globally ecological, demo- types (proteins and DNA, coding and noncoding levels). We graphic, and life history variables in 1,200 diverse species across have attempted a holistic, integrative analysis of the organism– life, thousands of populations, and tens of thousands of individ- environment interaction in the twin evolutionary processes of uals tested mostly for allozyme and partly for DNA diversity. adaptation and speciation. Likewise, we tested thermal, chemical, climatic, and biotic stresses in several model organisms. Recently, we introduced genetic maps Problems EVOLUTION and quantitative trait loci to elucidate the genetic basis of adap- Major problems of evolutionary biology await solutions. They tation and speciation. The genome–phenome holistic model was can be resolved in a genomic era, when complete prokaryote and deciphered by the global regressive, progressive, and convergent eukaryote genomes are available for comparative analysis (1). A evolution of subterranean mammals. Our results indicate abun- major unresolved question is how much of the coding and dant genotypic and phenotypic diversity in nature. The organiza- noncoding genome diversity, the latter comprising Ͼ95% in tion and evolution of molecular and organismal diversity in nature eukaryotes, affects the twin evolutionary processes of adaptation at global, regional, and local scales are nonrandom and structured; and speciation. Furthermore, how much of this diversity in display regularities across life; and are positively correlated with, coding and particularly noncoding genomes, often called ‘‘junk’’ and partly predictable by, abiotic and biotic environmental heter- DNA, contributes to regulation and differential fitness of or- ogeneity and stress. Biodiversity evolution, even in small isolated ganisms and is subjected to natural selection? What proportion populations, is primarily driven by natural selection, including of observed genic and nongenic diversity is maintained by diversifying, balancing, cyclical, and purifying selective regimes, selection? How much of the diversity in noncoding DNA is interacting with, but ultimately overriding, the effects of mutation, adaptive and regulates gene expression, transcription, transla- migration, and stochasticity. tion, recombination, and repair? The adaptive nature of the Ecological Genomics: Extension of Ecological Genetics noncoding genome now turns out to be one of the most intriguing questions in evolutionary genetics, as was the case with the ong-Term Research Program in the Institute of Evolution. The coding genome during the last decades of the 20th century. Lgenomic revolution has dramatically opened wide horizons for evolutionary studies, linking molecular and organismal or- Methods and Ecological Testing Theaters. To answer the problems ganizational levels. Here, I primarily review the 1975–2000 of diversity in the coding and noncoding genome, it is not research program in the Institute of Evolution, University of sufficient to measure their genetic diversity. The estimates of Haifa. This program involves biodiversity evolution, from molecular diversity derived from PCR-based techniques—such bacteria to mammals, of genes, genomes, phenomes, popula- as amplified fragment length polymorphism (AFLP), microsat- tions, species, ecosystems, and biota as well as their intimate ellites (short sequence repeats or SSR), single nucleotide poly- reciprocal interaction with spatiotemporal variables and the morphism (SNP) and sequence comparisons—are several-fold stressful physical and biotic environments resulting in adaptation higher than enzymatic diversity. The elucidation and significance and speciation. of molecular diversity need critical examination, experiments, Our model organisms represent diverse taxa across life, from and mapping that relate to coded allozymes but particularly to bacteria to mammals, in an attempt to unravel regularity, noncoding DNA diversity and to explanatory attempts of DNA convergence, and divergence of genotypic and phenotypic pat- linguistics (ref. 2; V. M. Kirzhner, A. B. Korol, A. Bolshoy, and terns: Nostoc linckia (cyanobacterium); Sordaria fimicola (co- E.N., unpublished work). prophilous fungus); Triticum dicoccoides and Hordeum sponta- Essentially, we are attempting to elucidate the reciprocal neum (wild cereals); Drosophila melanogaster (fruit fly); Spalax relationships between organism and environment. This strategy ehrenbergi superspecies (blind subterranean mole rats); Acomys has been adopted by the school of ecological genetics (4). This cahirinus and Apodemus mystacinus (aboveground rodents). We also studied globally and regionally the population genetics of 1,200 species from bacteria to mammals, primarily based on Abbreviations: EC, evolution canyon; AFLP, amplified fragment length polymorphism; SNP, literature data and species richness of 3,000 species in the two single nucleotide polymorphism; SSR, short sequence repeats; RAPD, randomly amplified ‘‘evolution canyons’’ (ECs). polymorphic DNA; SFS, south-facing slope; NFS, north-facing slope. The aforementioned model organisms comprise haploids and *E-mail: [email protected]. www.pnas.org͞cgi͞doi͞10.1073͞pnas.101109298 PNAS ͉ May 22, 2001 ͉ vol. 98 ͉ no. 11 ͉ 6233–6240 Downloaded by guest on October 1, 2021 strategy guiding the research program of the Institute of Evo- able by, abiotic and biotic ecological heterogeneity (that is, lution (1975–2000) across life and diverse ecogeographical the- spatiotemporal variation in niche-width) and environmental aters, coupled with observations and critical experiments, stress, and is often negatively correlated with population size proved successful at global (5), regional (6), and local (7, 8) scales (11). These results are inconsistent with the predictions of the (reviewed in refs. 9–12) at the allozyme diversity level. The neutral theory of molecular evolution (13) and seem to be strategy has now been extended into the DNA coding and primarily driven by natural selection. Critical laboratory exper- noncoding genomes, thereby advancing the science of ecological iments with marine organisms subjected to pollution cause fast genomics. The major questions for allozymes, and now for the differential mortality of allozyme genotypes, indicating that they DNA coding and noncoding genome, relate to the organism– are selected by the environment (20). environment interaction. Is the diversity random or nonrandom? How does differential stress and niche-width affect genomic and The Adaptive Evolution of Enzyme Kinetic Diversity. Kinetic studies phenomic diversity? What are the genome–phenome relation- of hemoglobin, haptoglobin, transferrin proteins, and at least a ships? Does speciation necessarily entail large genomic changes? dozen enzyme polymorphisms typically reveal biochemical ki- netic differences among the gene products of alternative geno- Evidence types at a locus (16). These include single gene effects, such as Allozyme Diversity and Evolution. Darwin introduced natural se- lactate dehydrogenase in killifish, leucine aminopeptidase in lection as the major mechanism of evolution. But what propor- blue mussel, and phosphoglucose isomerase in Collias butter- tion of all genomic and phenomic evolutionary change results flies. Similar results were obtained with alcohol dehydrogenase from natural selection? The most striking population-genetic in fruit flies, salamanders, and barley; glutamate-pyruvate feature is the great and widespread allozyme diversity in nature transaminase in copepods; as well as esterase, glucose-6- across unrelated organisms from bacteria to mammals (9–12, phosphate, 6-phosphogluconate dehydrogenase, and superoxide 16–18). Can the study of origin and dynamics of genotypic and dismutase in fruit flies (16). In all these cases, biochemical- phenotypic diversity, within and between populations, demon- kinetic studies reveal differences among phenotypes,