A framework for the study of genetic variation in migratory behaviour

Evolutionary change results from selection acting on genetic variation. For migration to be successful, many different aspects of an animal’s physiology and behaviour need to function in a co-coordinated way. Changes in one migratory trait are therefore likely to be accompanied by changes in other migratory and life-history traits. At present, we have some knowledge of the pressures that operate at the various stages of migration, but we know very little about the extent of genetic variation in various aspects of the migratory syndrome. As a consequence, our ability to predict which species is capable of what kind of evolutionary change, and at which rate, is limited. Here, we review how our evolutionary understanding of migration may benefit from taking a quantitative-genetic approach and present a framework for studying the causes of phenotypic variation. We review past research, that has mainly studied single migratory traits in captive birds, and discuss how this work could be extended to study genetic variation in the wild and to account for genetic correlations and correlated selection. In the future, reaction-norm approaches may become very important, as they allow the study of genetic and environmental effects on phenotypic expression within a single framework, as well as of their interactions. We advocate making more use of repeated measurements on single individuals to study the causes of among-individual variation in the wild, as they are easier to obtain than data on relatives and can provide valuable information for identifying and selecting traits. This approach will be particularly informative if it involves systematic testing of individuals under different environmental conditions. We propose extending this research agenda by using optimality models to predict levels of variation and covariation among traits and constraints. This may help us to select traits in which we might expect genetic variation, and to identify the most informative environmental axes. We also recommend an expansion of the passerine model, as this model does not apply to birds, like geese, where cultural transmission of spatio-temporal information is an important determinant of migration patterns and their variation.     

Levels of genetic polymorphism: marker loci versus quantitative traits.

Species are the units used to measure ecological diversity and alleles are the units of genetic diversity. Genetic variation within and among species has been documented most extensively using allozyme electrophoresis. This reveals wide differences in genetic variability within, and genetic distances among, species, demonstrating that species are not equivalent units of diversity. The extent to which the pattern observed for allozymes can be used to infer patterns of genetic variation in quantitative traits depends on the forces generating and maintaining variability. Allozyme variation is probably not strictly neutral but, nevertheless, heterozygosity is expected to be influenced by population size and genetic distance will be affected by time since divergence. The same is true for quantitative traits influenced by many genes and under weak stabilizing selection. However, the limited data available suggest that allozyme variability is a poor predictor of genetic variation in quantitative traits within populations. It is a better predictor of general phenotypic divergence and of postzygotic isolation between populations or species, but is only weakly correlated with prezygotic isolation. Studies of grasshopper and planthopper mating signal variation and assortative mating illustrate how these characters evolve independently of general genetic and morphological variation. The role of such traits in prezygotic isolation, and hence speciation, means that they will contribute significantly to the diversity of levels of genetic variation within and among species.     

HOW SIMILAR ARE GENETIC CORRELATION STRUCTURES? DATA FROM MICE AND RATS

An integral assumption of many models of morphometric evolution is the equality of the genetic variance-covariance structure across evolutionary time. To examine this assumption, the quantitative-genetic aspects of morphometric form are examined for eight pelvic traits in laboratory rats (Rattus norvegicus) and random-bred ICR mice (Mus musculus). In both species, all traits are significantly heritable, and there are significant phenotypic and genetic correlations among traits, although environmental correlations among the eight traits are low. The size relations among the pelvic variables are isometric. Three matrix-permutation tests are used to examine similarity of phenotypic, genetic, and environmental covariance and correlation matrices within and between species. Independent patterns of morphometric covariation and correlation arise from genetic and environmental effects within each species and from environmental effects between species. The patterns of phenotypic and genetic covariation and correlation are similar within each species, and the phenotypic and genetic correlations are also similar between these species. However, genetic covariance matrices show no significant statistical association between species. It is suggested that the assumption of equality of genetic variance-covariance structures across divergent taxa should be approached with caution.     

The evolutionary ecology of alternative migratory tactics in salmonid fishes

Extensive individual variation in spatial behaviour is a common feature among species that exhibit migratory life cycles. Nowhere is this more evident than in salmonid fishes; individual fish may complete their entire life cycle in freshwater streams, others may migrate variable distances at sea and yet others limit their migrations to larger rivers or lakes before returning to freshwater streams to spawn. This review presents evidence that individual variation in migratory behaviour and physiology in salmonid fishes is controlled by developmental thresholds and that part of the variation in proximal traits activating the development of alternative migratory tactics is genetically based. We summarize evidence that alternative migratory tactics co‐exist within populations and that all individuals may potentially adopt any of the alternative phenotypes. Even though intra‐specific genetic divergence of migratory tactics is uncommon, it may occur if female competition for oviposition sites results in spawning segregation of alternative phenotypes. Because of their polygenic nature, alternative migratory tactics are considered as threshold traits. Threshold traits have two characteristics: an underlying 'liability' trait that varies in a continuous fashion, and a threshold value which is responsible for the discreetness observed in phenotypic distribution. We review evidence demonstrating that body size is an adequate proxy for the liability trait controlling the decision to migrate, but that the same phenotypic outcome (anadromy or residency) may be reached by different developmental pathways. The evidence suggesting a significant heritable component in the development of alternative migratory tactics is subsequently reviewed, leading us to conclude that alternative migratory tactics have considerable potential to respond to selection and evolve. We review what is known about the proximal physiological mechanisms mediating the translation of the continuous value of the liability trait into a discontinuous migratory tactic. We conclude by identifying several avenues for future research, including testing the frequency‐dependent selection hypothesis, establishing the relative importance of adaptive phenotypic plasticity in explaining some geographic gradients in migratory behaviour and identifying the physiological and genetic basis of the switching mechanisms responsible for alternative migratory tactics.     

Lessons learned from the dog genome

Extensive genetic resources and a high-quality genome sequence position the dog as an important model species for understanding genome evolution, population genetics and genes underlying complex phenotypic traits. Newly developed genomic resources have expanded our understanding of canine evolutionary history and dog origins. Domestication involved genetic contributions from multiple populations of gray wolves probably through backcrossing. More recently, the advent of controlled breeding practices has segregated genetic variability into distinct dog breeds that possess specific phenotypic traits. Consequently, genome-wide association and selective sweep scans now allow the discovery of genes underlying breed-specific characteristics. The dog is finally emerging as a novel resource for studying the genetic basis of complex traits, including behavior.     

A mother’s legacy: the strength of maternal effects in animal populations

Although mothers influence the traits of their offspring in many ways beyond the transmission of genes, it remains unclear how important such ‘maternal effects’ are to phenotypic differences among individuals. Synthesizing estimates derived from detailed pedigrees, we evaluated the amount of phenotypic variation determined by maternal effects in animal populations. Maternal effects account for half as much phenotypic variation within populations as do additive genetic effects. Maternal effects most greatly affect morphology and phenology but, surprisingly, are not stronger in species with prolonged maternal care than in species without. While maternal effects influence juvenile traits more than adult traits on average, they do not decline across ontogeny for behaviour or physiology, and they do not weaken across the life cycle in species without maternal care. These findings underscore maternal effects as an important source of phenotypic variation and emphasise their potential to affect many ecological and evolutionary processes.     

Speciation and rapid phenotypic differentiation in the yellow-rumped warbler Dendroica coronata complex

The relative importance of the Pleistocene glacial cycles in driving avian speciation remains controversial, partly because species limits in many groups remain poorly understood, and because current taxonomic designations are often based on phenotypic characteristics of uncertain phylogenetic significance. We use mtDNA sequence data to examine patterns of genetic variation, sequence divergence and phylogenetic relationships between phenotypically distinct groups of the yellow-rumped warbler complex. Currently classified as a single species, the complex is composed of two North American migratory forms (myrtle warbler Dendroica coronata coronata and Audubon's warbler Dendroica coronata auduboni), and two largely sedentary forms: Dendroica coronata nigrifrons of Mexico, and Dendroica coronata goldmani of Guatemala. The latter are typically considered to be races of the Audubon's warbler based on plumage characteristics. However, mtDNA sequence data reveal that sedentary Mesoamerican forms are reciprocally monophyletic to each other and to migratory forms, from which they show a long history of isolation. In contrast, migratory myrtle and Audubon's warblers form a single cluster due to high levels of shared ancestral polymorphism as evidenced by widespread sharing of mtDNA haplotypes despite marked phenotypic differentiation. Sedentary and migratory forms diverged in the early Pleistocene, whereas phenotypic differentiation between the two migratory forms has occurred in the Holocene and is likely the result of geographical isolation and subsequent range expansion since the last glaciation. Our results underscore the importance of Quaternary climatic events in driving songbird speciation and indicate that plumage traits can evolve remarkably fast, thus rendering them potentially misleading for inferring systematic relationships.     

Quantitative genetics of skeletal nonmetric traits in the rhesus macaques on Cayo Santiago. II. Phenotypic,genetic, and environmental correlations between traits

The general lack of phenotypic correlation among skeletal nonmetric traits has been interpreted as indicating a lack of genetic correlation among these traits. Nonmetric traits scored on animals in the skeletal collection of rhesus macaques from Cayo Santiago are used to calculate phenotypic, genetic, and environmental correlations between traits. The results show that even when phenotypic correlations are low, there may be large, significant genetic correlations among these traits. The genetic correlation pattern suggests that genes which affect nonmetric trait variation act primarily at a local level in the cranium, even though there are genes with pleiotropic effects on skeletal nonmetric traits throughout the cranium. Environmental and phenotypic correlations do not show this neighborhood pattern of correlation.     

The genetics of bird migration: stimulus, timing, and direction

The extent to which genetic factors are directly involved in the control of bird migration and the mode of inheritance involved has been studied systematically over the past 15 years in the Blackcap Sylvia atricapilla by cross-breeding and selective breeding. Results have also been obtained from a few experimental and field studies on Robins Eritfiacus rubecula, Blackbirds Turdus merula and Song Sparrows Melospiza melodia. Cross-breeding of migrants with nonmigrants has resulted in the partial transmission of migratory activity into the F, generation indicating that the urge to migrate is inherited and is based on a multilocus system with a threshold for expression. Migratoriness and sedentariness in obligate partial migrants is probably inherited in a similar way, suggesting that the decision to migrate also has a strong genetic basis. Both traits can be selected to phenotypic uniformity within 3–6 generations indicating an extremely high evolutionary potential. Orientation behaviour can also be transmitted to the offspring of a nonmigratory population by cross-breeding. Cross-breeding individuals with different migratory directions produced offspring with phenotypically intermediate directional preferences, suggesting that the migratory direction is also a predominantly heritable character. In the current development of novel migratory habits in those Central European Blackcaps that now winter in the British Isles, the inheritance of the novel migratory direction may be crucial. Genetic variation in migratory events seems to be sufficient to allow for many microevolutionary processes.     

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.     

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.     

Evolutionary Genetics of Animal Migration

Three primary approaches have been used to study the geneticsof migration: the analyses of population differences, of singlelocus effects, and of polygenic influences. Studies of populationsreared under similar conditions in "common garden" experimentsfrequently reveal gene effects contributing to differences inmigratory tendency. Single locus effects are known, but arenot common, a result to be expected given that migration iscomplex. Quantitative genetic studies reveal that heritabilitiesfor migration related traits are often high (approximately 0.5or more) suggesting significant amounts of genetic variationon which natural selection can act. Analyses of genetic correlationsdemonstrate that migratory behavior is part of a syndrome thatincludes aspects of both physiology and life history traits.The latter are characteristically those which contribute tocolonizing ability. Migratory behavior thus does not evolvein isolation. New migration patterns are still evolving, aswould be predicted from observed environmental changes and thegenetic variation present in migratory species.     

Quantitative trait loci mapping of phenotypic plasticity and genotype-environment interactions in plant and insect performance

Community genetic studies generally ignore the plasticity of the functional traits through which the effect is passed from individuals to the associated community. However, the ability of organisms to be phenotypically plastic allows them to rapidly adapt to changing environments and plasticity is commonly observed across all taxa. Owing to the fitness benefits of phenotypic plasticity, evolutionary biologists are interested in its genetic basis, which could explain how phenotypic plasticity is involved in the evolution of species interactions. Two current ideas exist: (i) phenotypic plasticity is caused by environmentally sensitive loci associated with a phenotype; (ii) phenotypic plasticity is caused by regulatory genes that simply influence the plasticity of a phenotype. Here, we designed a quantitative trait loci (QTL) mapping experiment to locate QTL on the barley genome associated with barley performance when the environment varies in the presence of aphids, and the composition of the rhizosphere. We simultaneously mapped aphid performance across variable rhizosphere environments. We mapped main effects, QTL × environment interaction (QTL×E), and phenotypic plasticity (measured as the difference in mean trait values) for barley and aphid performance onto the barley genome using an interval mapping procedure. We found that QTL associated with phenotypic plasticity were co-located with main effect QTL and QTL×E. We also located phenotypic plasticity QTL that were located separately from main effect QTL. These results support both of the current ideas of how phenotypic plasticity is genetically based and provide an initial insight into the functional genetic basis of how phenotypically plastic traits may still be important sources of community genetic effects.     

Association genetics of complex traits in plants

Association mapping is rapidly becoming the main method for dissecting the genetic architecture of complex traits in plants. Currently most association mapping studies in plants are preformed using sets of genes selected to be putative candidates for the trait of interest, but rapid developments in genomics will allow for genome-wide mapping in virtually any plant species in the near future. As the costs for genotyping are decreasing, the focus has shifted towards phenotyping. In plants, clonal replication and/or inbred lines allows for replicated phenotyping under many different environmental conditions. Reduced sequencing costs will increase the number of studies that use RNA sequencing data to perform expression quantitative trait locus (eQTL) mapping, which will increase our knowledge of how gene expression variation contributes to phenotypic variation. Current population sizes used in association mapping studies are modest in size and need to be greatly increased if mutations explaining less than a few per cent of the phenotypic variation are to be detected. Association mapping has started to yield insights into the genetic architecture of complex traits in plants, and future studies with greater genome coverage will help to elucidate how plants have managed to adapt to a wide variety of environmental conditions.     

GENETIC CORRELATIONS AMONG TRAITS DETERMINING MIGRATORY TENDENCY IN THE SAND CRICKET,GRYLLUS FIRMUS

Migration by flight is an important component of the life cycles of most insects. The probability that a given insect will migrate by flight is influenced by many factors, most notably the presence or absence of fully-developed wings and functional flight musculature. Considerable variation has also been reported in the flight propensity of fully-winged individuals with functional flight musculature. We test the hypothesis that these components of migratory tendency are genetically correlated in a wing-dimorhic cricket, Gryllus firmus. Flight propensity and condition of the dorsal longitudinal flight muscles (DLM) are examined in fully-winged (LW) crickets from lines selected for increasing and for decreasing %LW, as well as from unselected control lines. Increased %LW is found to be associated with increased flight propensity among individuals with intact DLM, and with retention of functional DLM. The opposite is true for lines selected for decreased %LW. These results indicate both phenotypic and genetic correlations among behavioral, physiological, and morphological traits determining migratory tendency. We propose that these correlations may result from the multifunctional role of juvenile hormone, which has been reported to influence wing development, flight muscle development and degeneration, and flight propensity. Finally, we discuss the potential influence of genetic correlations for migratory traits on the evolution and maintenance of migratory polymorphisms in insects.     

Genetic mapping and coccidial parasites: Past achievements and future prospects

Coccidial parasites including Cryptosporidium parvum, Cyclospora cayetanensis, Neospora caninum, Toxoplasma gondii and the Eimeria species can cause severe disease of medical and veterinary importance. As many as one-third of the human population may carry T. gondii infection, and Eimeria are thought to cost the global poultry production industry in excess of US$2 billion per annum. Despite their significance, effective vaccines are scarce and have been confined to the veterinary field. As sequencing and genotyping technologies continue to develop, genetic mapping remains a valuable tool for the identification of genes that underlie phenotypic traits of interest and the assembly of contiguous genome sequences. For the coccidian, cross-fertilization still requires in vivo infection, a feature of their life cycle which limits the use of genetic mapping strategies. Importantly, the development of population-based approaches has now removed the need to isolate clonal lines for genetic mapping of selectable traits, complementing the classical clone-based techniques. To date, four coccidial species, representing three genera, have been investigated using genetic mapping. In this review we will discuss recent progress with these species and examine the prospects for future initiatives.     

Genetic architecture of growth and body composition in unique chicken populations

A resource population was established by crossing one modern broiler sire from a commercial broiler breeder male line with dams from two unrelated highly inbred lines; F1 birds were intercrossed to produce two F2 populations. A variety of phe notypic measurements related to growth, muscling, internal organs, and skeleton were recorded for the F2 populations and contemporary pure inbred and broiler birds. Based on the means and phenotypic distributions of the F2 populations com pared to their parental lines, the effective number of genes affecting each trait and heterosis were estimated and discussed relative to the known genetic selection history for each trait. The results suggest that a high number of genes with small epistatic effects are involved in determining the phenotype for traits that broilers were traditionally selected for, and a lower number of genes with major effects are involved in determining the phenotype for traits related to fitness. The estimated number of genes and the phenotypic distributions of the different traits suggest that a quantitative trait loci (QTL) search might be more effectively applied for traits with a low number of involved genes and a high phenotypic distribution among the F2 birds than for traits that show a lower phenotypic distribution and a high number of genes.     

Genetic markers for stallion fertility--lessons from humans and mice

Our knowledge on the many aspects of mammalian reproduction in general and equine reproduction in particular has greatly increased during the last 15 years. Advances in the understanding of the physiology, cell biology, and biochemistry of reproduction have facilitated genetic analyses of fertility. Currently, there are more than 200 genes known that are involved in the production of fertile sperm cells. The completion of a number of mammalian genome projects will aid in the investigation of these genes in different species. Great progress has been made in the understanding of genetic aberrations that lead to male infertility. Additionally, the first genetic mechanisms are being discovered that contribute to the quantitative variation of fertility traits in fertile male animals. As artificial insemination (AI) represents a widespread technology in horse breeding, semen quality traits may eventually become an additional selection criterion for breeding stallions. Current research activities try to identify genetic markers that correlate to these semen quality traits. Here, we will review the current state of genetic research in male fertility and offer some perspectives for future research in horses.