ABSTRACT
Whether populations adapt to similar selection pressures using the same underlying genetic variants depends on population history and the distribution of standing genetic variation at the metapopulation level. Studies of sticklebacks provide a case in point: when colonizing and adapting to freshwater habitats, three-spined sticklebacks (Gasterosteus aculeatus) with high gene flow tend to fix the same adaptive alleles in the same major loci, whereas nine-spined sticklebacks (Pungitius pungitius) with limited gene flow tend to utilize a more heterogeneous set of loci. In accordance with this, we report results of quantitative trait locus (QTL) analyses using a backcross design showing that lateral plate number variation in the western European nine-spined sticklebacks mapped to 3 moderate-effect QTL, contrary to the major-effect QTL in three-spined sticklebacks and different from the 4 QTL previously identified in the eastern European nine-spined sticklebacks. Furthermore, several QTL were identified associated with variation in lateral plate size, and 3 moderate-effect QTL with body size. Together, these findings indicate more heterogenous and polygenic genetic underpinnings of skeletal armour variation in nine-spined than three-spined sticklebacks, indicating limited genetic parallelism underlying armour trait evolution in the family Gasterostidae.
Subject(s)
Quantitative Trait Loci , Smegmamorpha , Animals , Smegmamorpha/genetics , Genetic Variation , Male , Body Size/genetics , Female , PhenotypeABSTRACT
Additive and dominance genetic variances underlying the expression of quantitative traits are important quantities for predicting short-term responses to selection, but they are notoriously challenging to estimate in most non-model wild populations. Specifically, large-sized or panmictic populations may be characterized by low variance in genetic relatedness among individuals which, in turn, can prevent accurate estimation of quantitative genetic parameters. We used estimates of genome-wide identity-by-descent (IBD) sharing from autosomal SNP loci to estimate quantitative genetic parameters for ecologically important traits in nine-spined sticklebacks (Pungitius pungitius) from a large, outbred population. Using empirical and simulated datasets, with varying sample sizes and pedigree complexity, we assessed the performance of different crossing schemes in estimating additive genetic variance and heritability for all traits. We found that low variance in relatedness characteristic of wild outbred populations with high migration rate can impair the estimation of quantitative genetic parameters and bias heritability estimates downwards. On the other hand, the use of a half-sib/full-sib design allowed precise estimation of genetic variance components and revealed significant additive variance and heritability for all measured traits, with negligible dominance contributions. Genome-partitioning and QTL mapping analyses revealed that most traits had a polygenic basis and were controlled by genes at multiple chromosomes. Furthermore, different QTL contributed to variation in the same traits in different populations suggesting heterogeneous underpinnings of parallel evolution at the phenotypic level. Our results provide important guidelines for future studies aimed at estimating adaptive potential in the wild, particularly for those conducted in outbred large-sized populations.
Subject(s)
Genome , Multifactorial Inheritance , Humans , Genome/genetics , Chromosome Mapping , Phenotype , Models, Genetic , Polymorphism, Single Nucleotide/geneticsABSTRACT
Mutation rate is a fundamental parameter in population genetics. Apart from being an important scaling parameter for demographic and phylogenetic inference, it allows one to understand at what rate new genetic diversity is generated and what the expected level of genetic diversity is in a population at equilibrium. However, except for well-established model organisms, accurate estimates of de novo mutation rates are available for a very limited number of organisms from the wild. We estimated mutation rates (µ) in two marine populations of the nine-spined stickleback (Pungitius pungitius) with the aid of several 2- and 3-generational family pedigrees, deep (>50×) whole-genome resequences and a high-quality reference genome. After stringent filtering, we discovered 308 germline mutations in 106 offspring translating to µ = 4.83 × 10-9 and µ = 4.29 × 10-9 per base per generation in the two populations, respectively. Up to 20% of the mutations were shared by full-sibs showing that the level of parental mosaicism was relatively high. Since the estimated µ was 3.1 times smaller than the commonly used substitution rate, recalibration with µ led to substantial increase in estimated divergence times between different stickleback species. Our estimates of the de novo mutation rate should provide a useful resource for research focused on fish population genetics and that of sticklebacks in particular.
Subject(s)
Smegmamorpha , Animals , Smegmamorpha/genetics , Mutation Rate , Phylogeny , Mutation , Germ-Line MutationABSTRACT
Inbreeding depression refers to the reduced fitness of offspring produced by genetically-related individuals and is expected to be rare in large, outbred populations. When it occurs, marked fitness loss is possible as large populations can carry a substantial load of recessive harmful mutations which are normally sheltered at the heterozygous state. Using experimental cross data and genome-wide identity-by-descent (IBD) relationships from an outbred marine nine-spined stickleback (Pungitius pungitius) population, we documented a significant decrease in offspring survival probability with increasing parental IBD sharing associated with an average inbreeding load (B) of 10.5. Interestingly, we found that this relationship was also underlined by a positive effect of paternal inbreeding coefficient on offspring survival, suggesting that certain combinations of parental inbreeding and genetic relatedness among mates may promote offspring survival. Our results demonstrate the potential for substantial inbreeding load in an outbred population and emphasize the need to consider fine-scale genetic relatedness in future studies of inbreeding depression in the wild.
Subject(s)
Inbreeding Depression , Humans , Inbreeding Depression/genetics , Inbreeding , Mutation , Genome , HeterozygoteABSTRACT
The occurrence of similar phenotypes in multiple independent populations derived from common ancestral conditions (viz. parallel evolution) is a testimony of evolution by natural selection. Parallel evolution implies that populations share a common phenotypic response to a common selection pressure associated with habitat similarity. Examples of parallel evolution at genetic and phenotypic levels are fairly common, but the driving selective agents often remain elusive. Similarly, the role of phenotypic plasticity in facilitating early stages of parallel evolution is unclear. We investigated whether the relaxation of predation pressure associated with the colonization of freshwater ponds by nine-spined sticklebacks (Pungitius pungitius) likely explains the divergence in complex behaviors between marine and pond populations, and whether this divergence is parallel. Using laboratory-raised individuals exposed to different levels of perceived predation risk, we calculated vectors of phenotypic divergence for four behavioral traits between habitats and predation risk treatments. We found a significant correlation between the directions of evolutionary divergence and phenotypic plasticity, suggesting that divergence in behavior between habitats is aligned with the response to relaxation of predation pressure. Finally, we show alignment across multiple pairs of populations, and that relaxation of predation pressure has likely driven parallel evolution of behavior in this species.
Subject(s)
Smegmamorpha , Animals , Smegmamorpha/genetics , Predatory Behavior , Ecosystem , Selection, Genetic , Adaptation, PhysiologicalABSTRACT
Heritable variation in traits under natural selection is a prerequisite for evolutionary response. While it is recognized that trait heritability may vary spatially and temporally depending on which environmental conditions traits are expressed under, less is known about the possibility that genetic variance contributing to the expected selection response in a given trait may vary at different stages of ontogeny. Specifically, whether different loci underlie the expression of a trait throughout development and thus providing an additional source of variation for selection to act on in the wild, is unclear. Here we show that body size, an important life-history trait, is heritable throughout ontogeny in the nine-spined stickleback (Pungitius pungitius). Nevertheless, both analyses of quantitative trait loci and genetic correlations across ages show that different chromosomes/loci contribute to this heritability in different ontogenic time-points. This suggests that body size can respond to selection at different stages of ontogeny but that this response is determined by different loci at different points of development. Hence, our study provides important results regarding our understanding of the genetics of ontogeny and opens an interesting avenue of research for studying age-specific genetic architecture as a source of non-parallel evolution.
Subject(s)
Smegmamorpha , Animals , Body Size/genetics , Genetic Variation , Phenotype , Quantitative Trait Loci , Selection, Genetic , Smegmamorpha/physiologyABSTRACT
[This corrects the article DOI: 10.1098/rsos.191577.].
ABSTRACT
Phenotypic plasticity is an important mechanism allowing adaptation to new environments and as such it has been suggested to facilitate biological invasions. Under this assumption, invasive populations are predicted to exhibit stronger plastic responses than native populations. Drosophila suzukii is an invasive species whose males harbor a spot on the wing tip. In this study, by manipulating developmental temperature, we compare the phenotypic plasticity of wing spot size of two invasive populations with that of a native population. We then compare the results with data obtained from wild-caught flies from different natural populations. While both wing size and spot size are plastic to temperature, no difference in plasticity was detected between native and invasive populations, rejecting the hypothesis of a role of the wing-spot plasticity in the invasion success. In contrast, we observed a remarkable stability in the spot-to-wing ratio across temperatures, as well as among geographic populations. This stability suggests either that the spot relative size is under stabilizing selection, or that its variation might be constrained by a tight developmental correlation between spot size and wing size. Our data show that this correlation was lost at high temperature, leading to an increased variation in the relative spot size, particularly marked in the two invasive populations. This suggests: (a) that D. suzukii's development is impaired by hot temperatures, in agreement with the cold-adapted status of this species; (b) that the spot size can be decoupled from wing size, rejecting the hypothesis of an absolute constraint and suggesting that the wing color pattern might be under stabilizing (sexual) selection; and (c) that such sexual selection might be relaxed in the invasive populations. Finally, a subtle but consistent directional asymmetry in spot size was detected in favor of the right side in all populations and temperatures, possibly indicative of a lateralized sexual behavior.
ABSTRACT
Evidence is accumulating that evolutionary changes are not only common during biological invasions but may also contribute directly to invasion success. The genomic basis of such changes is still largely unexplored. Yet, understanding the genomic response to invasion may help to predict the conditions under which invasiveness can be enhanced or suppressed. Here, we characterized the genome response of the spotted wing drosophila Drosophila suzukii during the worldwide invasion of this pest insect species, by conducting a genome-wide association study to identify genes involved in adaptive processes during invasion. Genomic data from 22 population samples were analyzed to detect genetic variants associated with the status (invasive versus native) of the sampled populations based on a newly developed statistic, we called C2, that contrasts allele frequencies corrected for population structure. We evaluated this new statistical framework using simulated data sets and implemented it in an upgraded version of the program BayPass. We identified a relatively small set of single-nucleotide polymorphisms that show a highly significant association with the invasive status of D. suzukii populations. In particular, two genes, RhoGEF64C and cpo, contained single-nucleotide polymorphisms significantly associated with the invasive status in the two separate main invasion routes of D. suzukii. Our methodological approaches can be applied to any other invasive species, and more generally to any evolutionary model for species characterized by nonequilibrium demographic conditions for which binary covariables of interest can be defined at the population level.
Subject(s)
Adaptation, Biological , Drosophila/genetics , Genome, Insect , Introduced Species , Models, Genetic , Animals , Gene FrequencyABSTRACT
Phenotypic plasticity has been repeatedly suggested to facilitate adaptation to new environmental conditions, as in invasions. Here, we investigate this possibility by focusing on the worldwide invasion of Drosophila suzukii: an invasive species that has rapidly colonized all continents over the last decade. This species is characterized by a highly developed ovipositor, allowing females to lay eggs through the skin of ripe fruits. Using a novel approach based on the combined use of scanning electron microscopy and photogrammetry, we quantified the ovipositor size and three-dimensional shape, contrasting invasive and native populations raised at three different developmental temperatures. We found a small but significant effect of temperature and geographical origin on the ovipositor shape, showing the occurrence of both geographical differentiation and plasticity to temperature. The shape reaction norms are in turn strikingly similar among populations, suggesting very little difference in shape plasticity among invasive and native populations, and therefore rejecting the hypothesis of a particular role for the plasticity of the ovipositor in the invasion success. Overall, the ovipositor shape seems to be a fairly robust trait, indicative of stabilizing selection. The large performance spectrum rather than the flexibility of the ovipositor would thus contribute to the success of D. suzukii worldwide invasion.
ABSTRACT
Comparative studies of quantitative and neutral genetic differentiation (Q ST-F ST tests) provide means to detect adaptive population differentiation. However, Q ST-F ST tests can be overly liberal if the markers used deflate F ST below its expectation, or overly conservative if methodological biases lead to inflated F ST estimates. We investigated how marker type and filtering criteria for marker selection influence Q ST-F ST comparisons through their effects on F ST using simulations and empirical data on over 18 000 in silico genotyped microsatellites and 3.8 million single-locus polymorphism (SNP) loci from four populations of nine-spined sticklebacks (Pungitius pungitius). Empirical and simulated data revealed that F ST decreased with increasing marker variability, and was generally higher with SNPs than with microsatellites. The estimated baseline F ST levels were also sensitive to filtering criteria for SNPs: both minor alleles and linkage disequilibrium (LD) pruning influenced F ST estimation, as did marker ascertainment. However, in the case of stickleback data used here where Q ST is high, the choice of marker type, their genomic location, ascertainment and filtering made little difference to outcomes of Q ST-F ST tests. Nevertheless, we recommend that Q ST-F ST tests using microsatellites should discard the most variable loci, and those using SNPs should pay attention to marker ascertainment and properly account for LD before filtering SNPs. This may be especially important when level of quantitative trait differentiation is low and levels of neutral differentiation high.
ABSTRACT
Phenotypic plasticity has been proposed as a mechanism that facilitates the success of biological invasions. In order to test the hypothesis of an adaptive role for plasticity in invasions, particular attention should be paid to the relationship between the focal plastic trait, the environmental stimulus and the functional importance of the trait. The Drosophila wing is particularly amenable to experimental studies of phenotypic plasticity. Wing morphology is known for its plastic variation under different experimental temperatures, but this plasticity has rarely been investigated in a functional context of flight. Here, we investigate the effect of temperature on wing morphology and flight in the invasive pest species Drosophila suzukii Although the rapid invasion of both Europe and North America was most likely facilitated by human activities, D. suzukii is also expected to disperse actively. By quantifying wing morphology and individual flight trajectories of flies raised under different temperatures, we tested whether (1) invasive populations of D. suzukii show higher phenotypic plasticity than their native counterparts, and (2) wing plasticity affects flight parameters. Developmental temperature was found to affect both wing morphology and flight parameters (in particular speed and acceleration), leaving open the possibility of an adaptive value for wing plasticity. Our results show no difference in phenotypic plasticity between invasive and native populations, rejecting a role for wing plasticity in the invasion success.
Subject(s)
Adaptation, Physiological/physiology , Drosophila/growth & development , Flight, Animal/physiology , Temperature , Wings, Animal/growth & development , Animals , Introduced Species , MaleABSTRACT
Divergent selection may initiate ecological speciation extremely rapidly. How often and at what pace ecological speciation proceeds to yield strong reproductive isolation is more uncertain. Here, we document a case of extraordinarily rapid speciation associated with ecological selection in the postglacial Baltic Sea. European flounders (Platichthys flesus) in the Baltic exhibit two contrasting reproductive behaviors: pelagic and demersal spawning. Demersal spawning enables flounders to thrive in the low salinity of the Northern Baltic, where eggs cannot achieve neutral buoyancy. We show that demersal and pelagic flounders are a species pair arising from a recent event of speciation. Despite having a parapatric distribution with extensive overlap, the two species are reciprocally monophyletic and show strongly bimodal genotypic clustering and no evidence of contemporary migration, suggesting strong reproductive isolation. Divergence across the genome is weak but shows strong signatures of selection, a pattern suggestive of a recent ecological speciation event. We propose that spawning behavior in Baltic flounders is the trait under ecologically based selection causing reproductive isolation, directly implicating a process of ecological speciation. We evaluated different possible evolutionary scenarios under the approximate Bayesian computation framework and estimate that the speciation process started in allopatry â¼2,400 generations ago, following the colonization of the Baltic by the demersal lineage. This is faster than most known cases of ecological speciation and represents the most rapid event of speciation ever reported for any marine vertebrate.
Subject(s)
Flounder/genetics , Genetic Speciation , Animals , Biological Evolution , Ecology , Ecosystem , Fishes , Genome , Genomics/methods , Marine Biology/methods , Selection, GeneticABSTRACT
Deciphering invasion routes from molecular data is crucial to understanding biological invasions, including identifying bottlenecks in population size and admixture among distinct populations. Here, we unravel the invasion routes of the invasive pest Drosophila suzukii using a multi-locus microsatellite dataset (25 loci on 23 worldwide sampling locations). To do this, we use approximate Bayesian computation (ABC), which has improved the reconstruction of invasion routes, but can be computationally expensive. We use our study to illustrate the use of a new, more efficient, ABC method, ABC random forest (ABC-RF) and compare it to a standard ABC method (ABC-LDA). We find that Japan emerges as the most probable source of the earliest recorded invasion into Hawaii. Southeast China and Hawaii together are the most probable sources of populations in western North America, which then in turn served as sources for those in eastern North America. European populations are genetically more homogeneous than North American populations, and their most probable source is northeast China, with evidence of limited gene flow from the eastern US as well. All introduced populations passed through bottlenecks, and analyses reveal five distinct admixture events. These findings can inform hypotheses concerning how this species evolved between different and independent source and invasive populations. Methodological comparisons indicate that ABC-RF and ABC-LDA show concordant results if ABC-LDA is based on a large number of simulated datasets but that ABC-RF out-performs ABC-LDA when using a comparable and more manageable number of simulated datasets, especially when analyzing complex introduction scenarios.
Subject(s)
Bayes Theorem , Drosophila/genetics , Genetics, Population/methods , Phylogeography/methods , Animals , China , Computer Simulation , Genetic Variation/genetics , Genotype , Hawaii , Introduced Species , Japan , Microsatellite Repeats/genetics , Models, Genetic , North AmericaABSTRACT
The invasive pest Drosophila suzukii is characterized by a specific fresh-fruit targeting behavior and has quickly become a menace for the fruit economy of newly infested North American and European regions. D. suzukii carries a strain of the endosymbiotic bacterium Wolbachia, named wSuz, which has a low infection frequency and no reproductive manipulation capabilities in American populations of D. suzukii. To further understand the nature of wSuz biology and assess its utility as a tool for controlling this pest's populations, we investigated the prevalence of Wolbachia in 23 European D. suzukii populations, and compared our results with those available in American populations. Our data showed a highly variable infection frequency with a mean prevalence of 46%, which is significantly higher than the 17% found in American populations. Based on Multilocus Sequence Typing analysis, a single wSuz strain was diagnosed in all European populations of D. suzukii. In agreement with American data, we found no evidence of cytoplasmic incompatibility induced by wSuz. These findings raise two questions: a) why Wolbachia is maintained in field populations of D. suzukii and b) what are the selective forces responsible for the variation in prevalence within populations, particularly between European and American continents? Our results provide new insights into the D. suzukii-Wolbachia association and highlight regional variations that await further investigation and that should be taken into account for using Wolbachia-based pest management programs.
Subject(s)
Drosophila/microbiology , Wolbachia/physiology , Animals , Europe , Multilocus Sequence Typing , North America , Wolbachia/classification , Wolbachia/geneticsABSTRACT
The ancient fungus-growing termite (Mactrotermitinae) symbiosis involves the obligate association between a lineage of higher termites and basidiomycete Termitomyces cultivar fungi. Our investigation of the fungus-growing termite Macrotermes natalensis shows that Bacillus strains from M. natalensis colonies produce a single major antibiotic, bacillaene A (1), which selectively inhibits known and putatively antagonistic fungi of Termitomyces. Comparative analyses of the genomes of symbiotic Bacillus strains revealed that they are phylogenetically closely related to Bacillus subtilis, their genomes have high homology with more than 90% of ORFs being 100% identical, and the sequence identities across the biosynthetic gene cluster for bacillaene are higher between termite-associated strains than to the cluster previously reported in B. subtilis. Our findings suggest that this lineage of antibiotic-producing Bacillus may be a defensive symbiont involved in the protection of the fungus-growing termite cultivar.