Identification of selection signatures in livestock species

The identification of regions that have undergone selection is one of the principal goals of theoretical and applied evolutionary genetics. Such studies can also provide information about the evolutionary processes involved in shaping genomes, as well as physical and functional information about genes/genomic regions. Domestication followed by breed formation and selection schemes has allowed the formation of very diverse livestock breeds adapted to a wide variety of environments and with special characteristics. The advances in genomics in the last five years have enabled the development of several methods to detect selection signatures and have resulted in the publication of a considerable number of studies involving livestock species. The aims of this review are to describe the principal effects of natural/artificial selection on livestock genomes, to present the main methods used to detect selection signatures and to discuss some recent results in this area. This review should be useful also to research scientists working with wild animals/non-domesticated species and plant biologists working with breeding and evolutionary biology.     

Directional selection on initial flowering date in Phlox drummondii (Polemoniaceae)

The fitness effects due to initial flowering date in Phlox drummondii were determined for three populations in central Texas (USA) over 3 yr (1990-1992). Mean fitness (seed set) always decreased with the later initiation of flowering. The likelihood of a plant fruiting differed with flowering date in five of the six instances (population by year combinations). Though plants that initiated flowering later tended to have spent more time in the vegetative stage and tended to die later in the year than did earlier flowering plants, this was not sufficient to overcome the reproductive penalties of flowering late. Plants that initiated flowering later in the season spent less time in the adult phase and were smaller. The mean number of flowers, fruits, and seeds per flowering plant always decreased with later flowering. Fruit set was negatively correlated with flowering date in four of the six population by year combinations. Nonparametric fitness functions were used to summarize predicted fitness among different initial flowering dates for each population on a yearly basis. Predicted mean fitness always declined nonlinearly with later flowering; the earliest flowering plants always had the highest predicted fitness. These fitness functions describe directional selection for the early initiation of flowering.     

Detecting signatures of selection in nine distinct lines of broiler chickens

Modern commercial chickens have been bred for one of two specific purposes: meat production (broilers) or egg production (layers). This has led to large phenotypic changes, so that the genomic signatures of selection may be detectable using statistical techniques. Genetic differentiation between nine distinct broiler lines was calculated using Weir and Cockerham's pairwise F_ST estimator for 11 003 genome‐wide markers to identify regions showing evidence of differential selection across lines. Differentiation measures were averaged into overlapping sliding windows for each line, and a permutation approach was used to determine the significance of each window. A total of 51 regions were found to show significant differentiation between the lines. Several lines were consistently found to share significant regions, suggesting that the pattern of line divergence is related to selection for broiler traits. The majority of the 51 regions contain QTL relating to broiler traits, but only five of them were found to be significantly enriched for broiler QTL, including a region on chromosome 27 containing 39 broiler QTL and 114 genes. Additionally, a number of these regions have been identified by other selection mapping studies. This study has identified a large number of potential selection signatures, and further tests with higher‐density marker data may narrow these regions down to individual genes.     

Asymmetric reproductive character displacement in male aggregation behaviour

Reproductive character displacement--the evolution of traits that minimize reproductive interactions between species--can promote striking divergence in male signals or female mate preferences between populations that do and do not occur with heterospecifics. However, reproductive character displacement can affect other aspects of mating behaviour. Indeed, avoidance of heterospecific interactions might contribute to spatial (or temporal) aggregation of conspecifics. We examined this possibility in two species of hybridizing spadefoot toad (genus Spea). We found that in Spea bombifrons sympatric males were more likely than allopatric males to associate with calling males. Moreover, contrary to allopatric males, sympatric S. bombifrons males preferentially associated with conspecific male calls. By contrast, Spea multiplicata showed no differences between sympatry and allopatry in likelihood to associate with calling males. Further, sympatric and allopatric males did not differ in preference for conspecifics. However, allopatric S. multiplicata were more variable than sympatric males in their responses. Thus, in S. multiplicata, character displacement may have refined pre-existing aggregation behaviour. Our results suggest that heterospecific interactions can foster aggregative behaviour that might ultimately contribute to clustering of conspecifics. Such clustering can generate spatial or temporal segregation of reproductive activities among species and ultimately promote reproductive isolation.     

Asymmetrical reproductive character displacement in the house mouse

Our study addressed reproductive character displacement between two subspecies of the house mouse, Mus musculus musculus and Mus musculus domesticus that hybridize in Europe along a zone where selection against hybridization is known to occur. Based on a multi-population approach, we investigated spatial patterns of divergence of mate preference in the two taxa. Mate preference was significantly higher in the contact zone than in allopatry in both subspecies, suggesting that reproductive character displacement occurs. Moreover, patterns of preference were stronger in M. m. musculus than in M. m. domesticus, indicating an asymmetrical divergence between the two. In the context of selection against hybridization, our results may provide empirical support for the hypothesis of reinforcement in a parapatric hybrid zone. We discuss factors that could explain the asymmetrical pattern of divergence and the possible impact of a unimodal structure on the maintenance of premating divergence between the two subspecies.     

The evolution of reproductive character displacement conflicts with how sexual selection operates within a species

Processes that affect the evolution of female preferences or male display traits involved in mating decisions in different geographic areas have the potential to result in within-species divergence. This could occur via reinforcement of mate recognition in species using the same traits for species recognition and sexual selection. Sympatric individuals experience reinforcement of female preferences and male display traits, whereas allopatric individuals do not, creating the potential for divergent sexual selection in sympatric and allopatric populations. Sexual selection operates on the cuticular hydrocarbons (CHCs) of Drosophila serrata, and reinforcement on the CHCs of populations sympatric with D. birchii. Here, we manipulate sexual selection in D. serrata populations generated by hybridizing natural sympatric and allopatric populations. Under the influence of sexual selection, male CHCs evolved from an intermediate phenotype to resemble an allopatric phenotype, which was driven by female choice. Additionally, female choice resulted in evolution of an allopatric female preference, so that allopatric males were preferred to sympatric males. Allopatric CHCs and preferences represent a sexual selection optimum via female choice. Sympatric populations display suboptimal phenotypes relative to their allopatric conspecifics. The combination of reinforcement and sexual selection can therefore generate divergence in female preferences and male display traits.     

Revisiting the false positive rate in detecting recent positive selection

There is increasing interest in studying the molecular mechanisms of recent adaptations caused by positive selection in the genomics era. Such endeavors to detect recent positive selection, however, have been severely handicapped by false positives due to the confounding impact of demography and the population structure. To reduce false positives, it is critical to conduct a functional analysis to identify the true candidate genes/mutations from those that are filtered through neutrality tests. However, the extremely high cost of such functional analysis may restrict studies within a small number of model species. In particular, when the false positive rate of neutrality tests is high, the efficiency of the functional analysis will also be very low. Therefore, although the recent improvements have been made in the (joint) inference of demography and selection, our ultimate goal, which is to understand the mechanism of adaptation generally in a wide variety of natural populations, may not be achieved using the currently available approaches. More attention should thus be spent on the development of more reliable tests that could not only free themselves from the confounding impact of demography and the population structure but also have reasonable power to detect selection.     

Rapid sexual and genomic isolation in sympatric Drosophila without reproductive character displacement

The rapid evolution of sexual isolation in sympatry has long been associated with reinforcement (i.e., selection to avoid maladaptive hybridization). However, there are many species pairs in sympatry that have evolved rapid sexual isolation without known costs to hybridization. A major unresolved question is what evolutionary processes are involved in driving rapid speciation in such cases. Here, we focus on one such system; the Drosophila athabasca species complex, which is composed of three partially sympatric and interfertile semispecies: WN, EA, and EB. To study speciation in this species complex, we assayed sexual and genomic isolation within and between these semispecies in both sympatric and allopatric populations. First, we found no evidence of reproductive character displacement (RCD) in sympatric zones compared to distant allopatry. Instead, semispecies were virtually completely sexually isolated from each other across their entire ranges. Moreover, using spatial approaches and coalescent demographic simulations, we detected either zero or only weak heterospecific gene flow in sympatry. In contrast, within each semispecies we found only random mating and little population genetic structure, except between highly geographically distant populations. Finally, we determined that speciation in this system is at least an order of magnitude older than previously assumed, with WN diverging first, around 200K years ago, and EA and EB diverging 100K years ago. In total, these results suggest that these semispecies should be given full species status and we adopt new nomenclature: WN—D. athabasca, EA—D. mahican, and EB—D. lenape. While the lack of RCD in sympatry and interfertility do not support reinforcement, we discuss what additional evidence is needed to further decipher the mechanisms that caused rapid speciation in this species complex.     

A genome‐wide scan for selection signatures in Yorkshire and Landrace pigs based on sequencing data

Pigs have experienced dramatic selection due to domestication, which has led to many different phenotypes when compared to their wild counterparts, especially in the last several decades. Currently, genome‐wide scans in both cattle and humans showing positive selection footprints have been investigated. However, few studies have focused on porcine selection footprints, particularly on a genome‐wide scale. Surveying for selection footprints across porcine genomes can be quite valuable for revealing the genetic mechanisms of phenotypic diversity. Here, we employed a medium sequencing depth (5–20x/site per individual, on average) approach called genotyping by genome reducing and sequencing (GGRS) to detect genome‐wide selection signatures of two domestic pig breeds (Yorkshire and Landrace) that have been under intensive selection for traits of muscle development, growth and behavior. The relative extended haplotype homozygosity test, which identifies selection signatures by measuring the characteristics of haplotypes’ frequency distribution within a single population, was also applied to identify potential positively selected regions. As a result, signatures of positive selection were found in each breed. However, most selection signatures were population specific and related to genomic regions containing genes for biological categories including brain development, metabolism, growth and olfaction. Furthermore, the result of the gene set enrichment analysis indicated that selected regions of the two breeds presented a different over‐representation of genes in the Gene Ontology annotations and Kyoto Encyclopedia of Genes and Genomes pathways. Our results revealed a genome‐wide map of selection footprints in pigs and may help us better understand the mechanisms of selection in pig breeding.     

Using multilocus sequence data to assess population structure, natural selection, and linkage disequilibrium in wild tomatoes

We employed a multilocus approach to examine the effects of population subdivision and natural selection on DNA polymorphism in 2 closely related wild tomato species (Solanum peruvianum and Solanum chilense), using sequence data for 8 nuclear loci from populations across much of the species' range. Both species exhibit substantial levels of nucleotide variation. The species-wide level of silent nucleotide diversity is 18% higher in S. peruvianum (pi(sil) approximately 2.50%) than in S. chilense (pi(sil) approximately 2.12%). One of the loci deviates from neutral expectations, showing a clinal pattern of nucleotide diversity and haplotype structure in S. chilense. This geographic pattern of variation is suggestive of an incomplete (ongoing) selective sweep, but neutral explanations cannot be entirely dismissed. Both wild tomato species exhibit moderate levels of population differentiation (average F(ST) approximately 0.20). Interestingly, the pooled samples (across different demes) exhibit more negative Tajima's D and Fu and Li's D values; this marked excess of low-frequency polymorphism can only be explained by population (or range) expansion and is unlikely to be due to population structure per se. We thus propose that population structure and population/range expansion are among the most important evolutionary forces shaping patterns of nucleotide diversity within and among demes in these wild tomatoes. Patterns of population differentiation may also be impacted by soil seed banks and historical associations mediated by climatic cycles. Intragenic linkage disequilibrium (LD) decays very rapidly with physical distance, suggesting high recombination rates and effective population sizes in both species. The rapid decline of LD seems very promising for future association studies with the purpose of mapping functional variation in wild tomatoes.     

Positive selection versus demography: evolutionary inferences based on an unusual haplotype structure in Drosophila simulans

Coalescent simulations were used to investigate the possible role of population subdivision and history in shaping nucleotide variation in a recombining 88-kb genomic fragment of Drosophila simulans displaying an unusual large-scale haplotype structure. The multilocus analysis, based on summary statistics using specific demographic null models under recombination, indicates that the observed levels of linkage disequilibrium differed significantly from the values expected under different bottleneck and population admixture scenarios. These results indicate that demography alone may not account for the observed pattern of variation and support the previous claim that the data are better described by a model in which an adaptive mutation has not yet gone to fixation.     

Molecular evidence for selection on female color polymorphism in the damselfly Ischnura graellsii

The significance of female color polymorphism in Odonata remains controversial despite many field studies. The importance of random factors (founder effects, genetic drift and migration) versus selective forces for the maintenance of this polymorphism is still discussed. In this study, we specifically test whether the female color polymorphism of Ischnura graellsii (Odonata, Coenagrionidae) is under selection in the wild. We compared the degree of genetic differentiation based on RAPD markers (assumed to be neutral) with the degree of differentiation based on color alleles. Weir and Cockerham's theta values showed a significant degree of population differentiation for both sets of loci (RAPD and color alleles) but the estimated degree of population differentiation (theta) was significantly greater for the set of RAPD loci. This result shows that some sort of selection contributes to the maintenance of similar color morph frequencies across the studied populations. Our results combined with those of previous field studies suggest that at least in some I. graellsii populations, density-dependent mechanisms might help to prevent the loss of this polymorphism but cannot explain the similarity in morph frequencies among populations.     

Detection of selection signatures of population‐specific genomic regions selected during domestication process in Jinhua pigs

Chinese pigs have been undergoing both natural and artificial selection for thousands of years. Jinhua pigs are of great importance, as they can be a valuable model for exploring the genetic mechanisms linked to meat quality and other traits such as disease resistance, reproduction and production. The purpose of this study was to identify distinctive footprints of selection between Jinhua pigs and other breeds utilizing genome‐wide SNP data. Genotyping by genome reducing and sequencing was implemented in order to perform cross‐population extended haplotype homozygosity to reveal strong signatures of selection for those economically important traits. This work was performed at a 2% genome level, which comprised 152 006 SNPs genotyped in a total of 517 individuals. Population‐specific footprints of selective sweeps were searched for in the genome of Jinhua pigs using six native breeds and three European breeds as reference groups. Several candidate genes associated with meat quality, health and reproduction, such as GH1, CRHR2, TRAF4 and CCK, were found to be overlapping with the significantly positive outliers. Additionally, the results revealed that some genomic regions associated with meat quality, immune response and reproduction in Jinhua pigs have evolved directionally under domestication and subsequent selections. The identified genes and biological pathways in Jinhua pigs showed different selection patterns in comparison with the Chinese and European breeds.     

Parallel evolution and ecological selection: replicated character displacement in spadefoot toads

Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition''s role in divergent trait evolution.     

Genome‐wide analysis reveals artificial selection on coat colour and reproductive traits in Chinese domestic pigs

Pigs from Asia and Europe were independently domesticated from c. 9000 years ago. During this period, strong artificial selection has led to dramatic phenotypic changes in domestic pigs. However, the genetic basis underlying these morphological and behavioural adaptations is relatively unknown, particularly for indigenous Chinese pigs. Here, we performed a genome‐wide analysis to screen 196 regions with selective sweep signals in Tongcheng pigs, which are a typical indigenous Chinese breed. Genes located in these regions have been found to be involved in lipid metabolism, melanocyte differentiation, neural development and other biological processes, which coincide with the evolutionary phenotypic changes in this breed. A synonymous substitution, c.669T>C, in ESR1, which colocalizes with a major quantitative trait locus for litter size, shows extreme differences in allele frequency between Tongcheng pigs and wild boars. Notably, the variant C allele in this locus exhibits high allele frequency in most Chinese populations, suggesting a consequence of positive selection. Five genes (PRM1, PRM2, TNP2, GPR149 and JMJD1C) related to reproductive traits were found to have high haplotype similarity in Chinese breeds. Two selected genes, MITF and EDNRB, are implied to shape the two‐end black colour trait in Tongcheng pig. Subsequent SNP microarray studies of five Chinese white‐spotted breeds displayed a concordant signature at both loci, suggesting that these two genes are responsible for colour variations in Chinese breeds. Utilizing massively parallel sequencing, we characterized the candidate sites that adapt to artificial and environmental selections during the Chinese pig domestication. This study provides fundamental proof for further research on the evolutionary adaptation of Chinese pigs.     

Strong population structure characterizes weediness gene evolution in the invasive grass species Brachypodium distachyon

Mediterranean annual grasses have invaded California and have replaced vast areas of native grassland. One of these invasive grasses is Brachypodium distachyon , a new model species for the grasses with extensive genomic resources and a nearly completed genome sequence. This study shows that the level of genetic variation in invaded California grasslands is lower compared to the native range in Eurasia. The invaded regions are characterized by highly differentiated populations of B. distachyon isolated by distance, most likely as a result of founder effects and a dearth of outcrossing events. EXP6 and EXP10 encoding α-expansins responsible for rapid growth, and AGL11 and AGL13 encoding proteins involved in vegetative phase regulation, appear to be under purifying selection with no evidence for local adaptation. Our data show that B. distachyon has diverged only recently from related Brachypodium species and that tetraploidization might have been as recent as a few thousand years ago. Observed low genetic variation in EXP10 and AGL13 appears to have been present in Eurasia before tetraploidization, potentially as a result of strong selective pressures on advantageous mutations, which are most likely responsible for its fast growth and rapid completion of its life cycle.     

Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards

The pattern of reproductive character displacement (RCD)—in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation—is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40 years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A. caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.     

Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits-breeding habitat choice, timing of breeding, and plumage coloration-in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co-occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.