Biases in Demographic Modeling Affect Our Understanding of Recent Divergence

Testing among competing demographic models of divergence has become an important component of evolutionary research in model and non-model organisms. However, the effect of unaccounted demographic events on model choice and parameter estimation remains largely unexplored. Using extensive simulations, we demonstrate that under realistic divergence scenarios, failure to account for population size (N-e) changes in daughter and ancestral populations leads to strong biases in divergence time estimates as well as model choice. We illustrate these issues reconstructing the recent demographic history of North Sea and Baltic Sea turbots (Scophthalmus maximus) by testing 16 isolation with migration (IM) and 16 secondary contact (SC) scenarios, modeling changes in N-e as well as the effects of linked selection and barrier loci. Failure to account for changes in N-e resulted in selecting SC models with long periods of strict isolation and divergence times preceding the formation of the Baltic Sea. In contrast, models accounting for N-e changes suggest recent (Peer reviewe

From ecology to genetics and back: the tale of two flounder species in the Baltic Sea

Recent years have brought the realization that evolutionary changes driven by selection can occur in ecological time scales. However, recent evolutionary events can be hard to detect and may easily go unnoticed. For harvested species, such cryptic diversity may lead to suboptimal management. These points are illustrated by the two flounder species in the Baltic Sea. Although early ecological studies identified two ecotypes of European flounder (Platichthys flesus) based on spawning differences, genomic studies only recently demonstrated that they were reproductively isolated species, P. flesus and P. solemdali, separated through rapid ecologically driven speciation. These morphologically indistinguishable species are harvested within a mixed-stock fishery. In the northern Baltic Sea flounder landings have declined since the mid-1980s, with a drop in the Gulf of Finland (GoF) being particularly dramatic (∼90%). Genetic analyses of historical otolith samples from GoF catches have revealed that back in 1983 the fishery unknowingly targeted primarily P. flesus, whereas thereafter almost exclusively P. solemdali. Hence, the case of two flounder species illustrates (i) how ecological studies stimulated genetic investigations leading to discovery of ecological speciation and (ii) how cryptic species turnover discovered with genetic tools in turn improved ecological understanding with benefits to management and conservation.Peer reviewe

Allopatric origin of sympatric whitefish morphs with insights on the genetic basis of their reproductive isolation

The European whitefish (Coregonus lavaretus) species complex is a classic example of recent adaptive radiation. Here, we examine a whitefish population introduced to northern Finnish Lake Tsahkal in the late 1960s, where three divergent morphs (viz. littoral, pelagic, and profundal feeders) were found 10 generations after. Using demographic modeling based on genomic data, we show that whitefish morphs evolved during a phase of strict isolation, refuting a rapid sympatric divergence scenario. The lake is now an artificial hybrid zone between morphs originated in allopatry. Despite their current syntopy, clear genetic differentiation remains between two of the three morphs. Using admixture mapping, we identify five SNPs associated with gonad weight variation, a proxy for sexual maturity and spawning time. We suggest that ecological adaptations in spawning time evolved in allopatry are currently maintaining partial reproductive isolation in the absence of other barriers to gene flow.Peer reviewe

Cryptic temporal changes in stock composition explain the decline of a flounder (Platichthys spp.) assemblage

Unobserved diversity, such as undetected genetic structure or the presence of cryptic species, is of concern for the conservation and management of global biodiversity in the face of threatening anthropogenic processes. For instance, unobserved diversity can lead to overestimation of maximum sustainable yields and therefore to overharvesting of the more vulnerable stock components within unrecognized mixed-stock fisheries. We used DNA from archival (otolith) samples to reconstruct the temporal (1976-2011) genetic makeup of two mixed-stock flounder fisheries in the angstrom land Sea (AS) and the Gulf of Finland (GoF). Both fisheries have hitherto been managed as a single stock of European flounders (Platichthys flesus), but were recently revealed to target two closely related species: the pelagic-spawning P. flesus and the newly described, demersal-spawning P. solemdali. While the AS and GoF fisheries were assumed to consist exclusively of P. solemdali, P. flesus dominated the GoF flounder assemblage (87% of total) in 1983, had disappeared (0%) by 1993, and remained in low proportions (10%-11%) thereafter. In the AS, P. solemdali dominated throughout the sampling period (>70%), and P. flesus remained in very low proportions after 1983. The disappearance of P. flesus from the GoF coincides in time with a dramatic (similar to 60%) decline in commercial landings and worsening environmental conditions in P. flesus' northernmost spawning ground, the Eastern Gotland Basin, in the preceding 4-6 years. These results are compatible with the hypothesis that P. flesus in the GoF is a sink population relying on larval subsidies from southern spawning grounds and the cause of their disappearance is a cessation of larval supply. Our results highlight the importance of uncovering unobserved genetic diversity and studying spatiotemporal changes in the relative contribution of different stock components, as well as the underlying environmental causes, to manage marine resources in the age of rapid anthropogenic change.Peer reviewe

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 as 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 Clade’), and another that is comprised of populations from northern Europe and the east coast of North America (‘Trans-Atlantic Clade’). 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.Peer reviewe

Cast Away in the Adriatic: Low Degree of Parallel Genetic Differentiation in Three-Spined Sticklebacks

The three-spined stickleback (Gasterosteus aculeatus) has repeatedly and independently adapted to freshwater habitats from standing genetic variation (SGV) following colonization from the sea. However, in the Mediterranean Sea G. aculeatus is believed to have gone extinct, and thus the spread of locally adapted alleles between different freshwater populations via the sea since then has been highly unlikely. This is expected to limit parallel evolution, that is the extent to which phylogenetically related alleles can be shared among independently colonized freshwater populations. Using whole genome and 2b-RAD sequencing data, we compared levels of genetic differentiation and genetic parallelism of 15 Adriatic stickleback populations to 19 Pacific, Atlantic and Caspian populations, where gene flow between freshwater populations across extant marine populations is still possible. Our findings support previous studies suggesting that Adriatic populations are highly differentiated (average F-ST approximate to 0.45), of low genetic diversity and connectivity, and likely to stem from multiple independent colonizations during the Pleistocene. Linkage disequilibrium network analyses in combination with linear mixed models nevertheless revealed several parallel marine-freshwater differentiated genomic regions, although still not to the extent observed elsewhere in the world. We hypothesize that current levels of genetic parallelism in the Adriatic lineages are a relic of freshwater adaptation from SGV prior to the extinction of marine sticklebacks in the Mediterranean that has persisted despite substantial genetic drift experienced by the Adriatic stickleback isolates.Peer reviewe

Estimating uncertainty in divergence times among three-spined stickleback clades using the multispecies coalescent

Incomplete lineage sorting (ILS) can lead to biased divergence time estimates. To explore if and how ILS has influenced the results of a recent study of worldwide phylogeny of three-spined sticklebacks (Gasterosteus aculeatus), we estimated divergence times among major clades by applying both a concatenation approach and the multispecies coalescent (MSC) model to single-nucleotide polymorphisms. To further test the influence of different calibration strategies, we applied different calibrations to the root and to younger nodes in addition to the ones used in the previous study. Both the updated calibrations and the application of the MSC model influenced divergence time estimates, sometimes significantly. The new divergence time estimates were more ancient than in the previous study for older nodes, whereas the estimates of younger nodes were not strongly affected by the re-analyses. However, given the applied MSC method employs a simple substitution model and cannot account for changes in population size, we suggest that different analytical approaches and calibration strategies should be used in order to explore uncertainty in divergence time estimates. This study provides a valuable reference timeline for the ages of worldwide three-spined stickleback populations and emphasizes the need to embrace, rather than obscure, uncertainties around divergence time estimates.Peer reviewe

Identifying barriers to gene flow and hierarchical conservation units from seascape genomics : a modelling framework applied to a marine predator

The ongoing decline of large marine vertebrates must be urgently mitigated, particularly under increasing levels of climate change and other anthropogenic pressures. However, characterizing the connectivity among populations remains one of the greatest challenges for the effective conservation of an increasing number of endangered species. Achieving conservation targets requires an understanding of which seascape features influence dispersal and subsequent genetic structure. This is particularly challenging for adult-disperser species, and when distribution-wide sampling is difficult. Here, we developed a two-step modelling framework to investigate how seascape features drive the genetic connectivity of marine species without larval dispersal, to better guide the design of marine protected area networks and corridors. We applied this framework to the endangered grey reef shark, Carcharhinus amblyrhynchos, a reef-associated shark distributed across the tropical Indo-Pacific. In the first step, we developed a seascape genomic approach based on isolation-by-resistance models involving circuit theory applied to 515 shark samples, genotyped for 4991 nuclear single-nucleotide polymorphisms. We show that deep oceanic areas act as strong barriers to dispersal, while proximity to habitat facilitates dispersal. In the second step, we predicted the resulting genetic differentiation across the entire distribution range of the species, providing both local and global-scale conservation units for future management guidance. We found that grey reef shark populations are more fragmented than expected for such a mobile species, raising concerns about the resilience of isolated populations under high anthropogenic pressures. We recommend the use of this framework to identify barriers to gene flow and to help in the delineation of conservation units at different scales, together with its integration across multiple species when considering marine spatial planning.Peer reviewe

The roles of climate, geography and natural selection as drivers of genetic and phenotypic differentiation in a widespread amphibian Hyla annectans (Anura: Hylidae)

The role of geological events and Pleistocene climatic fluctuations as drivers of current patterns of genetic variation in extant species has been a topic of continued interest among evolutionary biologists. Nevertheless, comprehensive studies of widely distributed species are still rare, especially from Asia. Using geographically extensive sampling of many individuals and a large number of nuclear single nucleotide polymorphisms (SNPs), we studied the phylogeography and historical demography ofHyla annectanspopulations in southern China. Thirty-five sampled populations were grouped into seven clearly defined genetic clusters that closely match phenotype-based subspecies classification. These lineages diverged 2.32-5.23 million years ago (Ma), a timing that closely aligns with the rapid and drastic uplifting of the Qinghai-Tibet Plateau and adjacent southwest China. Demographic analyses and species distribution models indicate that different populations of this species have responded differently to past climatic changes. In the Hengduan Mountains, most populations experienced a bottleneck, whereas the populations located outside of the Hengduan Mountains have gradually declined in size since the end of the last glaciation. In addition, the levels of phenotypic and genetic divergence were strongly correlated across major clades. These results highlight the combined effects of geological events and past climatic fluctuations, as well as natural selection, as drivers of contemporary patterns of genetic and phenotypic variation in a widely distributed anuran in Asia.Peer reviewe