Daniel Berner

Genome divergence during evolutionary diversification as revealed in replicate lake-stream stickleback population pairs.

Evolutionary diversification is often initiated by adaptive divergence between populations occupying ecologically distinct environments while still exchanging genes. The genetic foundations of this divergence process are largely unknown and are here explored through genome scans in multiple independent lake-stream population pairs of threespine stickleback. We find that across the pairs, overall genomic divergence is associated with the magnitude of divergence in phenotypes known to be under divergent selection. Along this same axis of increasing diversification, genomic divergence becomes increasingly biased towards the centre of chromosomes as opposed to the peripheries. We explain this pattern by within-chromosome variation in the physical extent of hitchhiking, as recombination is greatly reduced in chromosome centres. Correcting for this effect suggests that a great number of genes distributed widely across the genome are involved in the divergence into lake vs. stream habitats. Analyzing additional allopatric population pairs, however, reveals that strong divergence in some genomic regions has been driven by selection unrelated to lake-stream ecology. Our study highlights a major contribution of large-scale variation in recombination rate to generating heterogeneous genomic divergence and indicates that elucidating the genetic basis of adaptive divergence might be more challenging than currently recognized.

Variable Progress Toward Ecological Speciation in Parapatry: Stickleback Across Eight Lake-Stream Transitions

Divergent selection between contrasting habitats can sometimes drive adaptive divergence and the evolution of reproductive isolation in the face of initially high gene flow. “Progress” along this ecological speciation pathway can range from minimal divergence to full speciation. We examine this variation for threespine stickleback fish that evolved independently across eight lake-stream habitat transitions. By quantifying stickleback diets, we show that lake-stream transitions usually coincide with limnetic-benthic ecotones. By measuring genetically based phenotypes, we show that these ecotones often generate adaptive divergence in foraging morphology. By analyzing neutral genetic markers (microsatellites), we show that adaptive divergence is often associated with the presence of two populations maintaining at least partial reproductive isolation in parapatry. Coalescent-based simulations further suggest that these populations have diverged with gene flow within a few thousand generations, although we cannot rule out the possibility of phases of allopatric divergence. Finally, we find striking variation among the eight lake-stream transitions in progress toward ecological speciation. This variation allows us to hypothesize that progress is generally promoted by strong divergent selection and limited dispersal across the habitat transitions. Our study thus makes a case for ecological speciation in a parapatric context, while also highlighting variation in the outcome.

Along the speciation continuum in sticklebacks

Speciation can be viewed as a continuum, potentially divisible into several states: (1) continuous variation within panmictic populations, (2) partially discontinuous variation with minor reproductive isolation, (3) strongly discontinuous variation with strong but reversible reproductive isolation and (4) complete and irreversible reproductive isolation. Research on sticklebacks (Gasterosteidae) reveals factors that influence progress back and forth along this continuum, as well as transitions between the states. Most populations exist in state 1, even though some of these show evidence of disruptive selection and positive assortative mating. Transitions to state 2 seem to usually involve strong divergent selection coupled with at least a bit of geographic separation, such as parapatry (e.g. lake and stream pairs and mud and lava pairs) or allopatry (e.g. different lakes). Transitions to state 3 can occur when allopatric or parapatric populations that evolved under strong divergent selection come into secondary contact (most obviously the sympatric benthic and limnetic pairs), but might also occur between populations that remained in parapatry or allopatry. Transitions to state 4 might be decoupled from these selective processes, because the known situations of complete, or nearly complete, reproductive isolation (Japan Sea and Pacific Ocean pair and the recognized gasterosteid species) are always associated with chromosomal rearrangements and environment-independent genetic incompatibilities. Research on sticklebacks has thus revealed complex and shifting interactions between selection, adaptation, mutation and geography during the course of speciation.

Natural selection drives patterns of lake–stream divergence in stickleback foraging morphology

To what extent are patterns of biological diversification determined by natural selection? We addressed this question by exploring divergence in foraging morphology of threespine stickleback fish inhabiting lake and stream habitats within eight independent watersheds. We found that lake fish generally displayed more developed gill structures and had more streamlined bodies than did stream fish. Diet analysis revealed that these morphological differences were associated with limnetic vs. benthic foraging modes, and that the extent of morphological divergence within watersheds reflected differences in prey resources utilized by lake and stream fish. We also found that patterns of divergence were unrelated to patterns of phenotypic trait (co)variance within populations (i.e. the ‘line of least resistance’). Instead, phenotypic (co)variances were more likely to have been shaped by adaptation to lake vs. stream habitats. Our study thus implicates natural selection as a strong deterministic force driving morphological diversification in lake–stream stickleback. The strength of this inference was obtained by complementing a standard analysis of parallel divergence in means between discrete habitat categories (lake vs. stream) with quantitative estimates of selective forces and information on trait (co)variances.

Recombination in the threespine stickleback genome—patterns and consequences

Heterogeneity in recombination rate may strongly influence genome evolution and entail methodological challenges to genomic investigation. Nevertheless, a solid understanding of these issues awaits detailed information across a broad range of taxa. Based on 282 F2 individuals and 1872 single nucleotide polymorphisms, we characterize recombination in the threespine stickleback fish genome. We find an average genome‐wide recombination rate of 3.11 cm/Mb. Crossover frequencies are dramatically elevated in the chromosome peripheries as compared to the centres, and are consistent with one obligate crossover per chromosome (but not chromosome arm). Along the sex chromosome, we show that recombination is restricted to a small pseudoautosomal domain of c. 2 Mb, spanning only 10% of that chromosome. Comparing female to male RAD sequence coverage allows us to identify two discrete levels of degeneration on the Y chromosome, one of these ‘evolutionary strata’ coinciding with a previously inferred inverted region. Using polymorphism data from two young (<10 000 years old) ecologically diverged lake‐stream population pairs, we demonstrate that recombination rate correlates with both the magnitude of allele frequency shifts between populations and levels of genetic diversity within populations. These associations reflect genome‐wide heterogeneity in the influence of selection on linked sites. We further find a strong relationship between recombination rate and GC content, possibly driven by GC‐biased gene conversion. Overall, we highlight that heterogeneity in recombination rate has profound consequences on genome evolution and deserves wider recognition in marker‐based genomic analyses.

The genomic signature of parallel adaptation from shared genetic variation.

Parallel adaptation is common and may often occur from shared genetic variation, but the genomic consequences of this process remain poorly understood. We first use individual-based simulations to demonstrate that comparisons between populations adapted in parallel to similar environments from shared variation reveal a characteristic genomic signature around a selected locus: a low-divergence valley centred at the locus and flanked by twin peaks of high divergence. This signature is initiated by the hitchhiking of haplotype tracts differing between derived populations in the broader neighbourhood of the selected locus (driving the high-divergence twin peaks) and shared haplotype tracts in the tight neighbourhood of the locus (driving the low-divergence valley). This initial hitchhiking signature is reinforced over time because the selected locus acts as a barrier to gene flow from the source to the derived populations, thus promoting divergence by drift in its close neighbourhood. We next empirically confirm the peak-valley-peak signature by combining targeted and RAD sequence data at three candidate adaptation genes in multiple marine (source) and freshwater (derived) populations of threespine stickleback. Finally, we use a genome-wide screen for the peak-valley-peak signature to discover additional genome regions involved in parallel marine-freshwater divergence. Our findings offer a new explanation for heterogeneous genomic divergence and thus challenge the standard view that peaks in population divergence harbour divergently selected loci and that low-divergence regions result from balancing selection or localized introgression. We anticipate that genome scans for peak-valley-peak divergence signatures will promote the discovery of adaptation genes in other organisms.

Size correction in biology: how reliable are approaches based on (common) principal component analysis?

Morphological traits typically scale with the overall body size of an organism. A meaningful comparison of trait values among individuals or populations that differ in size therefore requires size correction. A frequently applied size correction method involves subjecting the set of n morphological traits of interest to (common) principal component analysis [(C)PCA], and treating the first principal component [(C)PC1] as a latent size variable. The remaining variation (PC2–PCn) is considered size-independent and interpreted biologically. I here analyze simulated data and natural datasets to demonstrate that this (C)PCA-based size correction generates systematic statistical artifacts. Artifacts arise even when all traits are tightly correlated with overall size, and they are particularly strong when the magnitude of variance is heterogeneous among the traits, and when the traits under study are few. (C)PCA-based approaches are therefore inappropriate for size correction and should be abandoned in favor of methods using univariate general linear models with an adequate independent body size metric as covariate. As I demonstrate, (C)PC1 extracted from a subset of traits, not themselves subjected to size correction, can provide such a size metric.

Constraints on speciation suggested by comparing lake‐stream stickleback divergence across two continents

Adaptation to ecologically distinct environments can coincide with the emergence of reproductive barriers. The outcome of this process is highly variable and can range along a continuum from weak population differentiation all the way to complete, genome‐wide divergence. The factors determining how far diverging taxa will move along this continuum remain poorly understood but are most profitably investigated in taxa under replicate divergence. Here, we explore determinants of progress towards speciation by comparing phenotypic and molecular divergence within young (<150 years) lake‐stream stickleback pairs from Central Europe to divergence in older (thousands of years) archetypal lake‐stream pairs from Vancouver Island, Canada. We generally find relatively weak divergence in most aspects of foraging morphology (gill raker number, body shape) in the European pairs, although substantial adaptive divergence is seen in gill raker length. Combined with striking overall phenotypic differences between the continents, this argues for genetic and time constraints on adaptive divergence in the European pairs. The European lake‐stream pairs also do not display the strong habitat‐related differentiation in neutral (microsatellite) markers seen in the Canadian watersheds. This indicates either the lack of strong reproductive barriers owing to weak adaptive divergence, or alternatively that neutral markers are poorly suited for detecting reproductive barriers if these emerge rapidly. Overall, our comparative approach suggests constraints on speciation due to genetic architecture and limited time for divergence. The relative importance of these factors remains to be quantified by future investigation.

Uninformative polymorphisms bias genome scans for signatures of selection

BackgroundWith the establishment of high-throughput sequencing technologies and new methods for rapid and extensive single nucleotide (SNP) discovery, marker-based genome scans in search of signatures of divergent selection between populations occupying ecologically distinct environments are becoming increasingly popular.Methods and ResultsOn the basis of genome-wide SNP marker data generated by RAD sequencing of lake and stream stickleback populations, we show that the outcome of such studies can be systematically biased if markers with a low minor allele frequency are included in the analysis. The reason is that these ‘uninformative’ polymorphisms lack the adequate potential to capture signatures of drift and hitchhiking, the focal processes in ecological genome scans. Bias associated with uninformative polymorphisms is not eliminated by just avoiding technical artifacts in the data (PCR and sequencing errors), as a high proportion of SNPs with a low minor allele frequency is a general biological feature of natural populations.ConclusionsWe suggest that uninformative markers should be excluded from genome scans based on empirical criteria derived from careful inspection of the data, and that these criteria should be reported explicitly. Together, this should increase the quality and comparability of genome scans, and hence promote our understanding of the processes driving genomic differentiation.

The genomics of ecological vicariance in threespine stickleback fish.

Populations occurring in similar habitats and displaying similar phenotypes are increasingly used to explore parallel evolution at the molecular level. This generally ignores the possibility that parallel evolution can be mimicked by the fragmentation of an ancestral population followed by genetic exchange with ecologically different populations. Here we demonstrate such an ecological vicariance scenario in multiple stream populations of threespine stickleback fish divergent from a single adjacent lake population. On the basis of demographic and population genomic analyses, we infer the initial spread of a stream-adapted ancestor followed by the emergence of a lake-adapted population, that selective sweeps have occurred mainly in the lake population, that adaptive lake–stream divergence is maintained in the face of gene flow from the lake into the streams, and that this divergence involves major inversion polymorphisms also important to marine-freshwater stickleback divergence. Overall, our study highlights the need for a robust understanding of the demographic and selective history in evolutionary investigations.