The genomics of trait combinations and their influence on adaptive divergence

ABSTRACTUnderstanding rapid adaptation requires quantifying natural selection on traits and elucidating the genotype-phenotype relationship for those traits. However, recent studies have often failed to predict the direction of adaptive allelic variation in natural populations from laboratory studies. Here, we test for genomic signatures of genetic correlations to illustrate how multifarious, correlational selection may drive counterintuitive patterns of population divergence in the apple maggot fly, Rhagoletis pomonella (Diptera: Tephritidae). Apple-infesting populations with relatively early emerging adults have recently evolved from hawthorn-infesting populations consisting of relatively later emerging adults. Multiple studies have reported a paradoxical relationship between population differentiation and seasonal timing, as determined by the timing of diapause termination; alleles associated with late termination occur at higher frequencies in the earlier emerging apple-infesting populations compared to hawthorn-infesting populations. We present evidence that historical selection on diapause termination and another trait, initial diapause intensity, over geographic gradients generated genetic correlations between the traits in a direction antagonistic to contemporary selection on apple-infesting populations. Single nucleotide polymorphism in genomic regions of high linkage disequilibrium associated strongly with diapause termination and intensity, population divergence, geography, and evolutionary responses in laboratory selection experiments. These associations were consistent with geographically variable selection and with correlated evolutionary responses driving higher frequencies of late-associated alleles in the early emerging apple race. In contrast, loci associated only with diapause termination showed the expected pattern (more early-associated alleles in the apple race) in half of the population pairs. Our results suggest that selection on loci demonstrating antagonistic pleiotropy may often shape genomic footprints of rapid adaptation.

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Evolution of genetic variance during adaptive radiation

10.1101/097642 ◽

2017 ◽

Cited By ~ 3

Author(s):

Greg M. Walter ◽

J. David Aguirre ◽

Mark W. Blows ◽

Daniel Ortiz-Barrientos

Keyword(s):

Natural Selection ◽

Adaptive Radiation ◽

Genetic Variance ◽

Allelic Variation ◽

Genetic Correlations ◽

Leaf Traits ◽

Adaptive Divergence ◽

Ecotypic Differentiation ◽

Divergent Natural Selection ◽

Rapid Divergence

AbstractGenetic correlations between traits can bias adaptation away from optimal phenotypes and constrain the rate of evolution. If genetic correlations between traits limit adaptation to contrasting environments, rapid adaptive divergence across a heterogeneous landscape may be difficult. However, if genetic variance can evolve and align with the direction of natural selection, then abundant allelic variation can promote rapid divergence during adaptive radiation. Here, we explored adaptive divergence among ecotypes of an Australian native wildflower by quantifying divergence in multivariate phenotypes of populations that occupy four contrasting environments. We investigated differences in multivariate genetic variance underlying morphological traits and examined the alignment between divergence in phenotype and divergence in genetic variance. We found that divergence in mean multivariate phenotype has occurred along two major axes represented by different combinations of plant architecture and leaf traits. Ecotypes also showed divergence in the level of genetic variance in individual traits, and the multivariate distribution of genetic variance among traits. Divergence in multivariate phenotypic mean aligned with divergence in genetic variance, with most of the divergence in phenotype among ecotypes associated with a change in trait combinations that had substantial levels of genetic variance in each ecotype. Overall, our results suggest that divergent natural selection acting on high levels of standing genetic variation might fuel ecotypic differentiation during the early stages of adaptive radiation.

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Multiple chromosomal inversions contribute to adaptive divergence of a dune sunflower ecotype

10.1101/829622 ◽

2019 ◽

Cited By ~ 3

Author(s):

Kaichi Huang ◽

Rose L. Andrew ◽

Gregory L. Owens ◽

Kate L. Ostevik ◽

Loren H. Rieseberg

Keyword(s):

Natural Populations ◽

High Linkage Disequilibrium ◽

Adaptive Divergence ◽

Sequencing Data ◽

Association Analyses ◽

Chromosomal Inversions ◽

Sand Sheet ◽

Genomic Regions ◽

Helianthus Petiolaris ◽

Comparative Genetic Mapping

ABSTRACTBoth models and case studies suggest that chromosomal inversions can facilitate adaptation and speciation in the presence of gene flow by suppressing recombination between locally adapted alleles. Until recently, however, it has been laborious and time-consuming to identify and genotype inversions in natural populations. Here we apply RAD sequencing data and newly developed population genomic approaches to identify putative inversions that differentiate a sand dune ecotype of the prairie sunflower (Helianthus petiolaris) from populations found on the adjacent sand sheet. We detected seven large genomic regions that exhibit a different population structure than the rest of the genome and that vary in frequency between dune and non-dune populations. These regions also show high linkage disequilibrium and high heterozygosity between, but not within haplotypes, consistent with the behavior of large inversions, an inference subsequently validated in part by comparative genetic mapping. Genome-environment association analyses show that key environmental variables, including vegetation cover and soil nitrogen, are significantly associated with inversions. The inversions co-locate with previously described “islands of differentiation,” and appear to play an important role in adaptive divergence and incipient speciation within H. petiolaris.

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Nucleotide sequences of highly repeated DNAs; compilation and comments

Genetics Research ◽

10.1017/s0016672300020711 ◽

1982 ◽

Vol 39 (1) ◽

pp. 1-30 ◽

Cited By ~ 33

Author(s):

George L. Gabor Miklos ◽

Amanda Clare Gill

Keyword(s):

Satellite Dna ◽

Germ Line ◽

Sequence Data ◽

Allelic Variation ◽

Neutral Theory ◽

Natural Populations ◽

Evolutionary Significance ◽

Nucleotide Sequence Data ◽

A Genome ◽

Repeated Dnas

SummaryThe nucleotide sequence data from highly repeated DNAs of inverte-brates and mammals are summarized and briefly discussed. Very similar conclusions can be drawn from the two data bases. Sequence complexities can vary from 2 bp to at least 359 bp in invertebrates and from 3 bp to at least 2350 bp in mammals. The larger sequences may or may not exhibit a substructure. Significant sequence variation occurs for any given repeated array within a species, but the sources of this heterogeneity have not been systematically partitioned. The types of alterations in a basic repeating unit can involve base changes as well as deletions or additions which can vary from 1 bp to at least 98 bp in length. These changes indicate that sequence per se is unlikely to be under significant biological constraints and may sensibly be examined by analogy to Kimura's neutral theory for allelic variation. It is not possible with the present evidence to discriminate between the roles of neutral and selective mechanisms in the evolution of highly repeated DNA.Tandemly repeated arrays are constantly subjected to cycles of amplification and deletion by mechanisms for which the available data stem largely from ribosomal genes. It is a matter of conjecture whether the solutions to the mechanistic puzzles involved in amplification or rapid redeployment of satellite sequences throughout a genome will necessarily give any insight into biological functions.The lack of significant somatic effects when the satellite DNA content of a genome is significantly perturbed indicates that the hunt for specific functions at the cellular level is unlikely to prove profitable.The presence or in some cases the amount of satellite DNA on a chromosome, however, can have significant effects in the germ line. There the data show that localized condensed chromatin, rich in satellite DNA, can have the effect of rendering adjacent euchromatic regions rec−, or of altering levels of recombination on different chromosomes. No data stemming from natural populations however are yet available to tell us if these effects are of adaptive or evolutionary significance.

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Rapid, ultra-local adaptation facilitated by phenotypic plasticity

10.1101/598292 ◽

2019 ◽

Author(s):

Syuan-Jyun Sun ◽

Andrew M. Catherall ◽

Sonia Pascoal ◽

Benjamin J. M. Jarrett ◽

Sara E. Miller ◽

...

Keyword(s):

Gene Flow ◽

Rapid Evolution ◽

Reaction Norm ◽

Ancestral Population ◽

Adaptive Divergence ◽

Wild Populations ◽

Rapid Adaptation ◽

Burying Beetles ◽

Genetic Accommodation ◽

Nicrophorus Vespilloides

AbstractModels of ‘plasticity-first’ evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can still facilitate rapid evolution when diverging populations are connected by gene flow. Here we show how plasticity has generated adaptive divergence in fecundity in wild populations of burying beetlesNicrophorus vespilloides, which are still connected by gene flow, which occupy distinct Cambridgeshire woodlands that are just 2.5km apart and which diverged from a common ancestral population c. 1000-4000 years ago. We show that adaptive divergence is duetothe coupling of an evolved increase in the elevation of the reaction norm linking clutch size to carrion size (i.e. genetic accommodation) with plastic secondary elimination of surplus offspring. Working in combination, these two processes have facilitated rapid adaptation to fine-scale environmental differences, despite ongoing gene flow.

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Evolutionary inference from QST-FST comparisons: disentangling local adaptation from altitudinal gradient selection in snapdragon plants

10.1101/385377 ◽

2018 ◽

Cited By ~ 1

Author(s):

Sara Marin ◽

Juliette Archambeau ◽

Vincent Bonhomme ◽

Mylène Lascoste ◽

Benoit Pujol

Keyword(s):

Local Adaptation ◽

Natural Populations ◽

Common Garden ◽

Global Scale ◽

Structured Populations ◽

Adaptive Divergence ◽

Adaptation To Climate Change ◽

Phenotypic Differentiation ◽

Multiple Populations ◽

Environmental Demand

ABSTRACTPhenotypic differentiation among natural populations can be explained by natural selection or by neutral processes such as drift. There are many examples in the literature where comparing the effects of these processes on multiple populations has allowed the detection of local adaptation. However, these studies rarely identify the agents of selection. Whether population adaptive divergence is caused by local features of the environment, or by the environmental demand emerging at a more global scale, for example along altitudinal gradients, is a question that remains poorly investigated. Here, we measured neutral genetic (FST) and quantitative genetic (QST) differentiation among 13 populations of snapdragon plants (Antirrhinum majus) in a common garden experiment. We found low but significant genetic differentiation at putatively neutral markers, which supports the hypothesis of either ongoing pervasive homogenisation via gene flow between diverged populations or reproductive isolation between disconnected populations. Our results also support the hypothesis of local adaptation involving phenological, morphological, reproductive and functional traits. They also showed that phenotypic differentiation increased with altitude for traits reflecting the reproduction and the phenology of plants, thereby confirming the role of such traits in their adaptation to environmental differences associated with altitude. Our approach allowed us to identify candidate traits for the adaptation to climate change in snapdragon plants. Our findings imply that environmental conditions changing with altitude, such as the climatic envelope, influenced the adaptation of multiple populations of snapdragon plants on the top of their adaptation to local environmental features. They also have implications for the study of adaptive evolution in structured populations because they highlight the need to disentangle the adaptation of plant populations to climate envelopes and altitude from the confounding effects of selective pressures acting specifically at the local scale of a population.

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The molecular through ecological genetics of abnormal abdomen. IV. Components of genetic variation in a natural population of Drosophila mercatorum.

Genetics ◽

10.1093/genetics/130.2.355 ◽

1992 ◽

Vol 130 (2) ◽

pp. 355-366

Author(s):

H Hollocher ◽

A R Templeton ◽

R DeSalle ◽

J S Johnston

Keyword(s):

Genetic Variation ◽

Natural Population ◽

Allelic Variation ◽

Natural Populations ◽

Developmental Time ◽

Ecological Genetics ◽

Adult Longevity ◽

Genetic Determinants ◽

Drosophila Mercatorum ◽

Y Chromosomes

Abstract Natural populations of Drosophila mercatorum are polymorphic for a phenotypic syndrome known as abnormal abdomen (aa). This syndrome is characterized by a slow-down in egg-to-adult developmental time, retention of juvenile abdominal cuticle in the adult, increased early female fecundity, and decreased adult longevity. Previous studies revealed that the expression of this syndrome in females is controlled by two closely linked X chromosomal elements: the occurrence of an R1 insert in a third or more of the X-linked 28S ribosomal genes (rDNA), and the failure of replicative selection favoring uninserted 28S genes in larval polytene tissues. The expression of this syndrome in males in a laboratory stock was associated with the deletion of the rDNA normally found on the Y chromosome. In this paper we quantify the levels of genetic variation for these three components in a natural population of Drosophila mercatorum found near Kamuela, Hawaii. Extensive variation is found in the natural population for both of the X-linked components. Moreover, there is a significant association between variation in the proportion of R1 inserted 28S genes with allelic variation at the underreplication (ur) locus such that both of the necessary components for aa expression in females tend to cosegregate in the natural population. Accordingly, these two closely linked X chromosomal elements are behaving as a supergene in the natural population. Because of this association, we do not believe the R1 insert to be actively transposing to an appreciable extent. The Y chromosomes extracted from nature are also polymorphic, with 16% of the Ys lacking the Y-specific rDNA marker. The absence of this marker is significantly associated with the expression of aa in males. Hence, all three of the major genetic determinants of the abnormal abdomen syndrome are polymorphic in this natural population.

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Pleiotropic Meta-Analysis of Cognition, Education, and Schizophrenia Differentiates Roles of Early Neurodevelopmental and Adult Synaptic Pathways

10.1101/519967 ◽

2019 ◽

Cited By ~ 2

Author(s):

Max Lam ◽

W. David Hill ◽

Joey W. Trampush ◽

Jin Yu ◽

Emma Knowles ◽

...

Keyword(s):

Educational Attainment ◽

Cognitive Ability ◽

Genetic Correlation ◽

Allelic Variation ◽

Meta Analysis ◽

Genetic Correlations ◽

Biological Mechanisms ◽

Genetic Level ◽

Higher Educational Attainment ◽

Synaptic Pruning

AbstractLiability to schizophrenia is inversely correlated with general cognitive ability at both the phenotypic and genetic level. Paradoxically, a modest but consistent positive genetic correlation has been reported between schizophrenia and educational attainment, despite the strong positive genetic correlation between cognitive ability and educational attainment. Here we leverage published GWAS in cognitive ability, education, and schizophrenia to parse biological mechanisms underlying these results. Association analysis based on subsets (ASSET), a pleiotropic meta-analytic technique, allowed jointly associated loci to be identified and characterized. Specifically, we identified subsets of variants associated in the expected (“Concordant”) direction across all three phenotypes (i.e., greater risk for schizophrenia, lower cognitive ability, and lower educational attainment); these were contrasted with variants demonstrating the counterintuitive (“Discordant”) relationship between education and schizophrenia (i.e., greater risk for schizophrenia and higher educational attainment). ASSET analysis revealed 235 independent loci associated with cognitive ability, education and/or schizophrenia at p<5×10−8. Pleiotropic analysis successfully identified more than 100 loci that were not significant in the input GWASs, and many of these have been validated by larger, more recent single-phenotype GWAS. Leveraging the joint genetic correlations of cognitive ability, education, and schizophrenia, we were able to dissociate two distinct biological mechanisms: early neurodevelopmental pathways that characterize concordant allelic variation, and adulthood synaptic pruning pathways that were linked to the paradoxical positive genetic association between education and schizophrenia. Further, genetic correlation analyses revealed that these mechanisms contribute not only to the etiopathogenesis of schizophrenia, but also to the broader biological dimensions that are implicated in both general health outcomes and psychiatric illness.

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Population genomics of parallel hybrid zones in the mimetic butterflies, H. melpomene and H. erato

10.1101/000208 ◽

2013 ◽

Author(s):

Nicola Nadeau ◽

Mayte Ruiz ◽

Patricio Salazar ◽

Brian Counterman ◽

Jose Alejandro Medina ◽

...

Keyword(s):

Population Genomics ◽

De Novo ◽

Reference Sequence ◽

Colour Pattern ◽

Adaptive Divergence ◽

Population Divergence ◽

Hybrid Zones ◽

Data Alignment ◽

Parallel Hybrid ◽

Genomic Regions

Hybrid zones can be valuable tools for studying evolution and identifying genomic regions responsible for adaptive divergence and underlying phenotypic variation. Hybrid zones between subspecies of Heliconius butterflies can be very narrow and are maintained by strong selection acting on colour pattern. The co-mimetic species H. erato and H. melpomene have parallel hybrid zones where both species undergo a change from one colour pattern form to another. We use restriction associated DNA sequencing to obtain several thousand genome wide sequence markers and use these to analyse patterns of population divergence across two pairs of parallel hybrid zones in Peru and Ecuador. We compare two approaches for analysis of this type of data; alignment to a reference genome and de novo assembly, and find that alignment gives the best results for species both closely (H. melpomene) and distantly (H. erato, ~15% divergent) related to the reference sequence. Our results confirm that the colour pattern controlling loci account for the majority of divergent regions across the genome, but we also detect other divergent regions apparently unlinked to colour pattern differences. We also use association mapping to identify previously unmapped colour pattern loci, in particular the Ro locus. Finally, we identify within our sample a new cryptic population of H. timareta in Ecuador, which occurs at relatively low altitude and is mimetic with H. melpomene malleti.

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A quantitative genetic study of starvation resistance at different geographic scales in natural populations of Drosophila melanogaster

Genetics Research ◽

10.1017/s0016672310000327 ◽

2010 ◽

Vol 92 (4) ◽

pp. 253-259 ◽

Cited By ~ 12

Author(s):

JULIETA GOENAGA ◽

JUAN JOSÉ FANARA ◽

ESTEBAN HASSON

Keyword(s):

Drosophila Melanogaster ◽

Genetic Correlations ◽

Natural Populations ◽

Food Shortage ◽

Population Variation ◽

Phenotypic Variance ◽

Starvation Resistance ◽

Natural Genetic Variation ◽

Quantitative Genetic ◽

Variation Explained

SummaryFood shortage is a stress factor that commonly affects organisms in nature. Resistance to food shortage or starvation resistance (SR) is a complex quantitative trait with direct implications on fitness. However, surveys of natural genetic variation in SR at different geographic scales are scarce. Here, we have measured variation in SR in sets of lines derived from nine natural populations of Drosophila melanogaster collected in western Argentina. Our study shows that within population variation explained a larger proportion of overall phenotypic variance (80%) than among populations (7·2%). We also noticed that an important fraction of variation was sex-specific. Overall females were more resistant to starvation than males; however, the magnitude of the sexual dimorphism (SD) in SR varied among lines and explained a significant fraction of phenotypic variance in all populations. Estimates of cross-sex genetic correlations suggest that the genetic architecture of SR is only partially shared between sexes in the populations examined, thus, facilitating further evolution of the SD.

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