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opencc-by-4.0Aug 2022View details →

Complex population history affects admixture analyses in nine-spined sticklebacks

Genetic data and output files to reproduce the analyses from the manuscript :   TITLE: Complex population history affects admixture analyses in nine-spined sticklebacks AUTHORS: Xueyun Feng, Juha Merilä and Ari Löytynoja JOURNAL: Molecular Ecology YEAR: 2022 DOI: https://doi.org/10.1101/2021.07.16.452636 DATE: August 2, 2022   The Ninespine_phylogeography.zip folder contains the data and necessary output files to reproduce the analysis figures and tables in the above manuscript.

opencc-zeroAug 2022View details →

Data from: Relaxed risk of predation drives parallel evolution of stickleback behaviour

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 behaviours 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 behavioural 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 behaviour 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 behaviour in this species.

opencc-zeroAug 2022View details →

Sexually mediated phenotypic variation within and between sexes as a continuum structured by ecology: The mosaic nature of skeletal variation across body regions in Threespine stickleback (Gasterosteus aculeatus L.)

Ecological character displacement between the sexes, and sexual selection, integrate into a convergent set of factors that produce sexual variation. Ecologically-modulated, sexually mediated variation within and between sexes may be a major contributor to the amount of total variation that selection can act on in species. Threespine stickleback (Gasterosteus aculeatus) display rapid adaptive responses and sexual variation in many phenotypic traits. We examined phenotypic variation in the skull, pectoral and pelvic girdles of threespine stickleback from two freshwater and two coastal marine sites on the Sunshine Coast of British Columbia, Canada, using an approach that avoids a priori assumptions about bimodal patterns of variation. We quantified shape and size of the cranial, pectoral and pelvic regions of sticklebacks in marine and freshwater habitats using 3D geometric morphometrics and an index of sexually mediated variation. We show that the expression of phenotypic variation is structured in part by the effects of both habitat marine vs freshwater and the effects of individual sites within each habitat. Relative size exerts variable influence, and patterns of phenotypic variation associated with sex vary among body regions. This fine-grained quantification of sexually mediated variation in the context of habitat difference and different anatomical structures indicates a complex relationship between genetically inferred sex and environmental factors, demonstrating that the interplay between shared genetic background and sexually mediated, ecologically-based selective pressures structures the phenotypic expression of complex traits.

opencc-zeroMay 2024View details →

Data from: The transgenerational consequences of paternal social isolation and predation exposure in threespined sticklebacks

Parents routinely encounter stress in the ecological environment that can affect offspring development (transgenerational plasticity: TGP); however, parents' interactions with conspecifics may alter how parents respond to ecological stressors. During social buffering, the presence of conspecifics can reduce the response to or increase the speed of recovery from a stressor. This may have cascading effects on offspring if conspecifics can mitigate parental responses to ecological stress in ways that blunt the transmission of stress-induced transgenerational effects. Here, we simultaneously manipulated both paternal social isolation and experience with predation risk prior to fertilization in threespined stickleback (Gasterosteus aculeatus). We generated offspring via in-vitro fertilization to allow us to isolate paternal effects mediated via sperm alone (i.e., in the absence of paternal care). If social buffering mitigates TGP induced by paternal exposure to predation risk, then we expect the transgenerational effects of predation exposure to be weaker when a conspecific is present compared to when the father is isolated. Offspring of predator-exposed fathers showed reduced anxiety-like behavior and tended to be captured faster by the predator. Fathers who were socially isolated also had offspring that were captured faster by a live predator, suggesting that paternal social isolation may have maladaptive effects on how offspring respond to ecological stressors. Despite additive effects of paternal social isolation and paternal predation risk, we found no evidence of an interaction between these paternal treatments, suggesting that the presence of a conspecific did not buffer fathers and/or offspring from the effects of predation risk. Our results suggest that socially-induced stress is an important, yet underappreciated, mediator of TGP and can elicit transgenerational effects even in species that do not form permanent social groups. Future studies should therefore consider how the parental social environment can affect both within and trans-generational responses to ecological stressors.

Fig. 8 Fitness landscape for models 7 and 8 in Modelling sympatric speciation by means of biologically plausible mechanistic processes as exemplified by threespine stickleback species pairs

Fig. 8 Fitness landscape for models 7 and 8. Relative fitness is a function of trait T1 and trait T2. Epistasis is modelled as follows:

Fig. 5 The probability that a female accepts a in Modelling sympatric speciation by means of biologically plausible mechanistic processes as exemplified by threespine stickleback species pairs

Fig. 5 The probability that a female accepts a male as a mate is a function of the morphological difference between them, and her stringency of choosiness S (here T ¼ S þ 0: 25), as in model 4 (variants applied in models 6 and 8). In the figure, 3 values of S are shown; S can have all values that are averages of two allelic values (from 64 or 256 equidistant values from 0 to 1)

Fig. 3 Model 1. a in Modelling sympatric speciation by means of biologically plausible mechanistic processes as exemplified by threespine stickleback species pairs

Fig. 3 Model 1. a Typical initial distribution of the allelic values at generation 0. b Typical distribution of the allelic values at generation 100. c Typical distribution of T, the phenotypic values, at generation 100. Nm = Nf =100; σ =0.25; μ = 1%; n = 256 alleles. Similar results were obtained in 20 out of 20 replicate simulations with σ =0.25, in 13 out of 20 replicate simulations with σ =0.5, and in 0 out of 10 replicate simulations with σ =1

Fig. 6 Model 4 in Modelling sympatric speciation by means of biologically plausible mechanistic processes as exemplified by threespine stickleback species pairs

Fig. 6 Model 4: Reinforcement of stringency of assortative mating. Columns: 1 Typical distribution of morphology alleles; 2 typical distribution of morphology phenotypes T; 3 typical distribution of stringency of choosiness alleles. Rows: 1 Generation 0, 2 generation

opennotspecifiedJul 2023View details →

FIG. 3 in Rates of Alloparental Care by Male Stickleback in Natural Lake Populations

FIG. 3. Relationships between mismatch proportion and presence or absence of vegetation within 1 m of male stickleback nests across all lakes (n ¼ 15). Bold lines indicate significant lake trends (P, 0.05).

opennotspecifiedJul 2023View details →

FIG. 1 in Rates of Alloparental Care by Male Stickleback in Natural Lake Populations

FIG. 1. Frequency of alloparenting across lakes. Rates of mismatch (filled symbols) and 95% confidence intervals are shown with the total number of eggs tested for mismatch. Lakes are ordered from smallest to largest in surface area.

opennotspecifiedJul 2023View details →

FIG. 2 in Rates of Alloparental Care by Male Stickleback in Natural Lake Populations

FIG. 2. Mismatch probability based on male Z-d13C (a measure of diet, standardized to remove among-lake variation in mean and variance). Higher (less negative) values of Z- d13C indicate a more benthic diet; a bean plot shows the distribution while the tick marks represent individual data points.

opencc-zeroDec 2012View details →

Data from: The population structure and recent colonization history of Oregon threespine stickleback determined using restriction-site associated DNA-sequencing

Understanding how genetic variation is partitioned across genomes within and among populations is a fundamental problem in ecological and evolutionary genetics. To address this problem, we studied the threespine stickleback fish, which has repeatedly undergone parallel phenotypic and genetic differentiation when oceanic fish have invaded freshwater habitats. While significant evolutionary genetic research has been performed using stickleback from geographic regions that have been deglaciated in the last 20 000 years, less research has focused on freshwater populations that predate the last glacial maximum. We performed restriction-site associated DNA-sequencing (RAD-seq) based population genomic analyses on stickleback from across Oregon, which was not glaciated during the last maximum. We sampled stickleback from coastal, Willamette Basin and central Oregon sites, analysed their genetic diversity using RAD-seq, performed structure analyses, reconstructed their phylogeographic history and tested the hypothesis of recent stickleback introduction into central Oregon, where incidence of this species was only recently documented. Our results showed a clear phylogeographic break between coastal and inland populations, with oceanic populations exhibiting the lowest levels of divergence from one another. Willamette Basin and central Oregon populations formed a clade of closely related populations, a finding consistent with a recent introduction of stickleback into central Oregon. Finally, genome-wide analysis of genetic diversity (π) and correlations of alleles within individuals in subpopulations (FIS) supported a role for introgressive hybridization in coastal populations and a recent expansion in central Oregon. Our results exhibit the power of next-generation sequencing genomic approaches such as RAD-seq to identify both historical population structure and recent colonization history.

opencc-zeroOct 2019View details →

Widespread intersex differentiation across the stickleback genome – the signature of sexually antagonistic selection?

Females and males within a species commonly have distinct reproductive roles, and the associated traits may be under perpetual divergent natural selection between the sexes if their sex-specific control has not yet evolved. We here explore whether such sexually antagonistic selection can be detected based on the magnitude of differentiation between the sexes across genome-wide genetic polymorphisms by whole-genome sequencing of large pools of female and male threespine stickleback fish. We find numerous autosomal genome regions exhibiting intersex allele frequency differences beyond the range plausible under pure sampling stochasticity. Alternative sequence alignment strategies rule out that these high-differentiation regions represent sex chromosome segments misassembled into the autosomes. Instead, comparing allele frequencies and sequence read depth between the sexes reveals that regions of high intersex differentiation arise because autosomal chromosome segments got copied into the male-specific sex chromosome (Y), where they acquired new mutations. Because the Y chromosome is missing in the stickleback reference genome, sequence reads from derived DNA copies on the Y chromosome still align to the original homologous regions on the autosomes. We argue that this phenomenon hampers the identification of sexually antagonistic selection within a genome, and can lead to spurious conclusions from population genomic analyses when the underlying samples differ in sex ratios. Because the hemizygous sex chromosome sequence (Y or W) is not represented in most reference genomes, these problems may apply broadly.

opencc-zeroDec 2017View details →

Data from: Worldwide phylogeny of three-spined sticklebacks

Stickleback fishes in the family Gasterosteidae have become model organisms in ecology and evolutionary biology. However, even in the case of the most widely studied species in this family – the three-spined stickleback (Gasterosteus aculeatus) – the worldwide phylogenetic relationships and colonization history of the different populations and lineages remain poorly resolved. Using a large collection of samples covering most parts of the species distribution range, we subjected thousands of single nucleotide polymorphisms to coalescent analyses in order to reconstruct a robust worldwide phylogeny of extant G. aculeatus populations, as well their ancestral geographic distributions using Statistical-Dispersal Vicariance and Bayesian Binary MCMC analyses. The results suggest that contemporary populations originated from the Pacific Ocean in the late Pleistocene, and the Atlantic was colonized through the Arctic Ocean by a lineage that diverged from Pacific sticklebacks ca 44.6 Kya. This lineage contains two branches: one that is distributed in the Mediterranean area, from the Iberian Peninsula to the Black Sea ('Southern European lineage'), and another that is comprised of populations from northern Europe and the east coast of North America ('Trans-Atlantic lineage'). Hence, the results suggest that the North American East Coast was colonized by trans-Atlantic migration. Coalescence-based divergence time estimates suggest that divergence among major clades is much more recent than previously estimated.

opencc-zeroDec 2014View details →

Data from: Differences in rheotactic responses contribute to divergent habitat use between parapatric lake and stream threespine stickleback

Migration among populations is widely thought to undermine adaptive divergence, assuming gene flow arises from random movement of individuals. If individuals instead differ in dispersal behavior, phenotype-dependent dispersal can reduce the effective rate of gene flow or even facilitae divergence. For example, parapatric populations of lake and stream stickleback tend to actively avoid dispersing into the adjoining habitat.. However, the behavioral basis of this non-random dispersal was previously unknown. Here we show that lake and stream stickleback exhibit divergent rheotactic responses (behavioral response to currents). During the breeding season, wild-caught inlet stream stickleback were better than lake fish at maintaining position in currents, faced upstream more, and spent more time in low-current areas. As a result, stream fish expended significantly less energy in currents than did lake fish. These divergent rheotactic responses likely contribute to divergent habitat use by lake and stream stickleback. Although rheotactic differences were absent in non-breeding fish, divergent behavior of breeding-season fish may suffice for assortative mating by breeding location. The resulting reproductive isolation between lake and stream fish may explain the fine-scale evolutionary differentiation in parapatric stickleback populations.

opencc-zeroDec 2010View details →

Data from: Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation

Ecological selection against hybrids between populations occupying different habitats might be an important component of reproductive isolation during the initial stages of speciation. The strength and directionality of this barrier to gene flow depends on the genetic architecture underlying divergence in ecologically relevant phenotypes. We here present line cross analyses of inheritance for two key foraging-related morphological traits involved in adaptive divergence between stickleback ecotypes residing parapatrically in lake and stream habitats within the Misty Lake watershed (Vancouver Island, Canada). One main finding is striking genetic dominance of the lake phenotype for body depth. Selection associated with this phenotype against first and later generation hybrids should therefore be asymmetric, hindering introgression from the lake to the stream population but not vice versa. Another main finding is that divergence in gill raker number is inherited additively and should therefore contribute symmetrically to reproductive isolation. Our study suggests that traits involved in adaptation might contribute to reproductive isolation qualitatively differently, depending on their mode of inheritance.

opencc-zeroDec 2010View details →

Data from: Convergence and non-convergence in ecological, phenotypic, and genetic divergence across replicate population pairs of lake and stream stickleback

Convergent (or parallel) evolution provides strong evidence for a deterministic role of natural selection: similar phenotypes evolve when independent populations colonize similar environments. In reality, however, independent populations in similar environments always show some differences: some non-convergent evolution is present. It is therefore important to explicitly quantify the convergent and non-convergent aspects of trait variation, and to investigate the ecological and genetic explanations for each. We performed such an analysis for threespine stickleback (Gasterosteus aculeatus) populations inhabiting lake and stream habitats in independent watersheds. Morphological traits differed in the degree to which lake-stream divergence was convergent across watersheds. Some aspects of this variation were correlated with ecological variables related to diet, presumably reflecting the strength and specifics of divergent selection. Furthermore, a genetic scan revealed some markers that diverged between lakes and streams in many of the watersheds and some that diverged in only a few watersheds. Moreover, some of the lake-stream divergence in genetic markers was associated within some of the lake-stream divergence in morphological traits. Our results suggest that convergent evolution, and deviations from it, are primarily the result of natural selection, which corresponds in only some respect to the dichotomous habitat classifications frequently used in such studies.

opencc-zeroDec 2011View details →

Data from: Niche specialization influences adaptive phenotypic plasticity in threespine stickleback

Phenotypic plasticity may be favored in generalist populations if it increases niche width, even in temporally constant environments. Phenotypic plasticity can increase the frequency of extreme phenotypes in a population and thus allow it to make use of a wide resource spectrum. Here we test the prediction that generalist populations should be more plastic than specialists. In a common-garden experiment, we show that solitary, generalist populations of threespine sticklebacks inhabiting small coastal lakes of British Columbia have a higher degree of morphological plasticity than the more specialized sympatric limnetic and benthic species. The ancestral marine stickleback showed low levels of plasticity similar to those of sympatric sticklebacks, implying that the greater plasticity of the generalist population has evolved recently. Measurements of wild populations show that those with mean trait values intermediate between the benthic and limnetic values indeed have higher morphological variation. Our data indicate that plasticity can evolve rapidly after colonization of a new environment in response to changing niche use.

opencc-zeroDec 2012View details →

Data from: Weak habitat isolation in a threespine stickleback (Gasterosteus spp.) species pair

Reproductive isolation is central to the study of speciation. Multiple isolating barriers may prevent species from hybridizing, although their individual strength and the interactions between them are rarely measured. We quantified habitat isolation in a recently diverged threespine stickleback species pair (Gasterosteus aculeatus complex) and controlled for any such interactions. Using enclosures in an outdoor pond, we confirm that males of the two species strongly prefer different nesting habitats: limnetic males build nests in open habitats, whereas benthic males nest under vegetation. However, forcing males to nest in their nonpreferred habitat did not reduce the probability of spawning by females. As a result, habitat isolation between the species is estimated to be weak. We compared the strength of habitat isolation estimated in the present study with estimates of other behavioural barriers using previously published data. We discovered that, although total mating isolation between the species is strong, the contributions of differences in body size and male nuptial colour are similarly individually weak. Instead, interactions with other, undetermined species-specific traits were responsible for most of the isolation resulting from differences in body size and, in benthics, colour. This is one of the first attempts to estimate individual isolating barriers at the same time as controlling for interactions.