From population genetics to population genomics of forest trees: Integrated population genomics approach

Early works by Altukhov and his associates on pine and spruce laid the foundation for Russian population genetic studies on tree species with the use of molecular genetic markers. In recent years, these species have become especially popular as nontraditional eukaryotic models for population and evolutionary genome-wide research. Tree species with large, cross-pollinating native populations, high genetic and phenotypic variation, growing in diverse environments and affected by environmental changes during hundreds of years of their individual development, are an ideal model for studying the molecular genetic basis of adaptation. The great advance in this field is due to the rapid development of population genomics in the last few years. In the broad sense, population genomics is a novel, fast-developing discipline, combining traditional population genetic approaches with the genome-wide level of analysis. Thousands of genes with known function and sometimes known genome-wide localization can be simultaneously studied in many individuals. This opens new prospects for obtaining statistical estimates for a great number of genes and segregating elements. Mating system, gene exchange, reproductive population size, population disequilibrium, interaction among populations, and many other traditional problems of population genetics can be now studied using data on variation in many genes. Moreover, population genome-wide analysis allows one to distinguish factors that affect individual genes, allelles, or nucleotides (such as, for example, natural selection) from factors affecting the entire genome (e.g., demography). This paper presents a brief review of traditional methods of studying genetic variation in forest tree species and introduces a new, integrated population genomics approach. The main stages of the latter are: (1) selection of genes, which are tentatively involved in variation of adaptive traits, by means of a detailed examination of the regulation and the expression of individual genes and genotypes, with subsequent determination of their complete allelic composition by direct nucleotide sequencing; (2) examination of the phenotypic effects of individual alleles by, e.g., association mapping; and (3) determining the frequencies of the selected alleles in natural population for identification of the adaptive variation pattern in the heterogeneous environment. Through decoding the phenotypic effects of individual alleles and identification of adaptive variation patterns at the population level, population genomics in the future will serve as a very helpful, efficient, and economical tool, essential for developing a correct strategy for conserving and increasing forests and other commercially valuable plant and animal species.     

From population genetics to population genomics of forest trees: integrated population genomics approach

Early works by Altukhov and his associates on pine and spruce laid the foundation for Russian population genetic studies on tree species with the use of molecular genetic markers. In recent years, these species have become especially popular as nontraditional eukaryotic models for population and evolutionary genomic research. Tree species with large, cross-pollinating native populations, high genetic and phenotypic variation, growing in diverse environments and affected by environmental changes during hundreds of years of their individual development, are an ideal model for studying the molecular genetic basis of adaptation. The great advance in this field is due to the rapid development of population genomics in the last few years. In the broad sense, population genomics is a novel, fast-developing discipline, combining traditional population genetic approaches with the genomic level of analysis. Thousands of genes with known function and sometimes known genomic localization can be simultaneously studied in many individuals. This opens new prospects for obtaining statistical estimates for a great number of genes and segregating elements. Mating system, gene exchange, reproductive population size, population disequilibrium, interaction among populations, and many other traditional problems of population genetics can be now studied using data on variation in many genes. Moreover, population genomic analysis allows one to distinguish factors that affect individual genes, alleles, or nucleotides (such as, for example, natural selection) from factors affecting the entire genome (e.g., demography). This paper presents a brief review of traditional methods of studying genetic variation in forest tree species and introduces a new, integrated population genomics approach. The main stages of the latter are : (1) selection of genes, which are tentatively involved in variation of adaptive traits, by means of a detailed examination of the regulation and the expression of individual genes and genotypes, with subsequent determination of their complete allelic composition by direct nucleotide sequencing; (2) examination of the phenotypic effects of individual alleles by, e.g., association mapping; and (3) determining the frequencies of the selected alleles in natural population for identification of the adaptive variation pattern in the heterogeneous environment. Through decoding the phenotypic effects of individual alleles and identification of adaptive variation patterns at the population level, population genomics in the future will serve as a very helpful, efficient, and economical tool, essential for developing a correct strategy for conserving and increasing forests and other commercially valuable plant and animal species.     

Integrating population genetics and conservation biology in the era of genomics

As one of the final activities of the ESF-CONGEN Networking programme, a conference entitled ‘Integrating Population Genetics and Conservation Biology’ was held at Trondheim, Norway, from 23 to 26 May 2009. Conference speakers and poster presenters gave a display of the state-of-the-art developments in the field of conservation genetics. Over the five-year running period of the successful ESF-CONGEN Networking programme, much progress has been made in theoretical approaches, basic research on inbreeding depression and other genetic processes associated with habitat fragmentation and conservation issues, and with applying principles of conservation genetics in the conservation of many species. Future perspectives were also discussed in the conference, and it was concluded that conservation genetics is evolving into conservation genomics, while at the same time basic and applied research on threatened species and populations from a population genetic point of view continues to be emphasized.     

Crop evolution: from genetics to genomics

The advent of the genomics age has greatly facilitated the study of crop evolution. While full-scale genome sequencing projects are underway for just a handful of crop plants, recent years have witnessed a tremendous increase in the availability of DNA sequence data for virtually all major crops. Such resources have bolstered 'traditional' genetic approaches such as QTL mapping and candidate gene-based association studies. They have also allowed us to undertake genome-wide analyses in which we simultaneously consider the importance of a large and essentially random collection of genes. These sorts of analyses promise a more or less unbiased view of the genetic basis of crop evolution and will probably result in the identification of agronomically important genes that would have otherwise been overlooked.     

Approaches to prokaryotic biodiversity: a population genetics perspective

The study of prokaryotic diversity has blossomed during the last 10-15 years as a result of the introduction of molecular identification, mostly based on direct 16S rRNA gene polymerase chain reaction (PCR) amplification and sequencing from natural samples. A large amount of information exists about the diversity of this specific gene. However, data from the field of bacterial population genetics and genomics make questionable the value of information regarding just one gene. Even if we accept 16S rRNA genes as useful for species identification, intraspecific variation in bacteria is so high that species catalogues are often of little value. The gene pools represented by an operational species are yet impossible to predict. On the other hand, adaptive features in prokaryotes are often coded in gene clusters (genomic islands) that can be cloned directly from the environment, sequenced and even expressed in a surrogate host. Thus, the study of the environmental genome or metagenome appears as an alternative that could eventually lead to a more realistic understanding of prokaryotic biodiversity, provide biotechnology with new tools and maybe even contribute to develop a model of prokaryotic evolution.     

Marsupial genetics and genomics

Marsupials, the 'other' mammals, are found only in Australasia and the Americas. They are quite different from eutherian ('placental') mammals, as well they might be after 130 million years of separate evolution. They display a unique pattern of mammalian organization and development that is reflected by differences in their genomes. Here, we introduce marsupials as alternative (but not inferior!) mammals and summarize the state of knowledge of marsupial relationships, marsupial chromosomes, maps, genes and genetic regulatory systems. We shamelessly present the case for a Kangaroo Genome Project.     

Fragmentation genetics in tropical ecosystems: from fragmentation genetics to fragmentation genomics

Tropical regions are experiencing unprecedented economic and population growth. This goes hand in hand with increase habitat fragmentation of tropical ecosystems. Understanding the genetic consequences of these spatial and temporal changes across landscapes is critical to conservation of the vast majority of global biodiversity. This virtual issue of Conservation Genetics, presents six empirical and one review paper showcasing fascinating and important findings with regard to how habitat fragmentation impacts on genetic diversity in rare or endangered tropical species. The message from these papers is clear, fragmentation has a number of serious genetic consequences, which can contribute to undermining the viability of species in fragmented landscapes. Conservation genetics provides a powerful tool to inform both conservation and management of species and genetic resources. But, careful consideration is needed to ensure studies apply appropriate sampling designs and genetic analysis to better test hypothesis. Next generation genomics offers great opportunities to provide even more answers and greater resolution of the consequences for adaptive genetic variation, to ensure future tropical landscapes are resilient.     

Genotyping, gene genealogies and genomics bring fungal population genetics above ground

As ubiquitous decomposers, symbionts and parasites, fungi build populations not easily accommodated by population genetic theory. Identifying and delineating individuals and populations is often difficult, and recombination can occur in complex and variable ways. Genotyping and gene genealogies provide the framework for identifying and delineating individuals and for detecting recombination in natural populations. Expanding genomic databases now make fungi ideal subjects for tracking mutation and expression in genes of adaptive importance in experimental populations.     

A population genetics pedigree perspective on the transmission of Helicobacter pylori

The inference of transmission pathways for medicinally important bacteria is important to our understanding of pathogens. Here we report analyses of transmission in Helicobacter pylori, a major carcinogen. Our study is novel in that the focal community comprises detailed family pedigrees and has a high prevalence of H. pylori. To infer transmission, we performed high-resolution analyses of nucleotide sequences for three genes and accounted for the occurrence of mutation and recombination through the use of simulation modeling. Our results demonstrate that transmission has a strong nonfamilial component potentially the result of a large proportion of infections derived from the community. These results are interesting from both a medical and an evolutionary standpoint. First, efficient control measures and beliefs about the sources of H. pylori infection should be reevaluated. Evolutionarily, our results contradict the hypothesis of strict vertical transmission, presented as an explanation for the strong correlation between human population history and H. pylori diversity. Thus the paradox of persistent phylogenetic structure, despite a permissive mode of transmission and high recombination rates, must be solved elsewhere. Here we consider the potential for recombination events to maintain genetic structure in light of horizontal transmission.     

Population genetics from an information perspective

Some basic effects of population genetics are derived governing the occurrences of alleles A(i)and genotypes A(i)A(j)among its members. A principle of extreme physical information (EPI) is used. These effects are (1) the equation of genetic change, (2) Fisher's theorem of partial change, (3) a new uncertainty principle, and (4) the monotonic decrease of Fisher information with time, indicating increased disorder for the population. General conditions of population change are allowed: fitness coefficients w(ij)generally changing with time [except in effect (2)], population randomly or non-randomly mating, and a general number of loci present within each chromosome. EPI is a practical tool for deriving probability laws. It is an outgrowth of a physical process that occurs during any act of measurement. Here the measurement is the random observation of a genotype A(i)A(j). This observation is to be used to estimate the time of the observation, called "evolutionary time". The measurement activity incurs errors in the estimated observation time and fitness value of the observed genotype. By the Cramer-Rao inequality, the product of the two uncertainties must exceed unity [effect (3)]. The Fisher information I in data space is postulated to originate in the space of the genotype where it had some generally larger value J. The EPI principle extremizes the loss of information (I--J) with I=1/2 J. The solution gives rise to effects (1) and (2). Finally, it is shown that effect (4) holds when the population approaches an equilibrium state, e.g. for time values greater than a threshold if fitness coefficients w(ij)are constant. EPI provides a common framework for deriving physical laws and laws of population genetics. The new effects (3) and (4) are confirmed through computer simulation.     

Microbial diversity--insights from population genetics

Although many environmental microbial populations are large and genetically diverse, both the level of diversity and the extent to which it is ecologically relevant remain enigmatic. Because the effective (or long-term) population size, N_e, is one of the parameters that determines population genetic diversity, tests and simulations that assume selectively neutral mutations may help to identify the processes that have shaped microbial diversity. Using ecologically important genes, tests of selective neutrality suggest that adaptive as well as non-adaptive types of selection act and that departure from neutrality may be widespread or restricted to small groups of genotypes. Population genetic simulations using population sizes between 10³ and 10⁷ suggest extremely high levels of microbial diversity in environments that sustain large populations. However, census and effective population sizes may differ considerably, and because we know nothing of the evolutionary history of environmental microbial populations, we also have no idea what N_e of environmental populations is. On the one hand, this reflects our ignorance of the microbial world. On the other hand, the tests and simulations illustrate interactions between microbial diversity and microbial population genetics that should inform our thinking in microbial ecology. Because of the different views on microbial diversity across these disciplines, such interactions are crucial if we are to understand the role of genes in microbial communities.     

PGDSpider: an automated data conversion tool for connecting population genetics and genomics programs

The analysis of genetic data often requires a combination of several approaches using different and sometimes incompatible programs. In order to facilitate data exchange and file conversions between population genetics programs, we introduce PGDSpider, a Java program that can read 27 different file formats and export data into 29, partially overlapping, other file formats. The PGDSpider package includes both an intuitive graphical user interface and a command-line version allowing its integration in complex data analysis pipelines. AVAILABILITY: PGDSpider is freely available under the BSD 3-Clause license on http://cmpg.unibe.ch/software/PGDSpider/.     

Adaptive gene expression divergence inferred from population genomics

Detailed studies of individual genes have shown that gene expression divergence often results from adaptive evolution of regulatory sequence. Genome-wide analyses, however, have yet to unite patterns of gene expression with polymorphism and divergence to infer population genetic mechanisms underlying expression evolution. Here, we combined genomic expression data—analyzed in a phylogenetic context—with whole genome light-shotgun sequence data from six Drosophila simulans lines and reference sequences from D. melanogaster and D. yakuba. These data allowed us to use molecular population genetics to test for neutral versus adaptive gene expression divergence on a genomic scale. We identified recent and recurrent adaptive evolution along the D. simulans lineage by contrasting sequence polymorphism within D. simulans to divergence from D. melanogaster and D. yakuba. Genes that evolved higher levels of expression in D. simulans have experienced adaptive evolution of the associated 3′ flanking and amino acid sequence. Concomitantly, these genes are also decelerating in their rates of protein evolution, which is in agreement with the finding that highly expressed genes evolve slowly. Interestingly, adaptive evolution in 5′ cis-regulatory regions did not correspond strongly with expression evolution. Our results provide a genomic view of the intimate link between selection acting on a phenotype and associated genic evolution.