Genomic signatures of hybridization between Ixodes ricinus and Ixodes persulcatus in natural populations.

Identifying hybridization between common pathogen vectors is essential due to the major public health implications through risks associated with hybrid's enhanced pathogen transmission potential. The hard-ticks Ixodes ricinus and Ixodes persulcatus are the two most common vectors of tick-borne pathogens that affect human and animal health in Europe. Ixodes ricinus is a known native species in Finland with a well-known distribution, whereas I. persulcatus has expanded in range and abundance over the past 60 years, and currently it appears the most common tick species in certain areas in Finland. Here we used double-digest restriction site-associated DNA (ddRAD) sequencing on 186 ticks (morphologically identified as 92 I. ricinus, and 94 I. persulcatus) collected across Finland to investigate whether RAD generated single nucleotide polymorphisms (SNPs) can discriminate tick species and identify potential hybridization events. Two different clustering methods were used to assign specific species based on how they clustered and identified hybrids among them. We were able to discriminate between the two tick species and identified 11 putative hybrids with admixed genomic proportions ranging from approximately 24 to 76 percent. Four of these hybrids were morphologically identified as I. ricinus while the remaining seven were identified as I. persulcatus. Our results thus indicate that RAD SNPs are robust in identifying both species of the ticks as well as putative hybrids. These results further suggest ongoing hybridization between I. ricinus and I. persulcatus in their natural populations in Finland. The unique ability of RAD markers to discriminate between tick species and hybrids adds a useful aspect to tick evolutionary studies. Our findings align with previous studies and suggest a shared evolutionary history between the species, with instances of individuals possessing a considerable proportion of the other species' genome. This study is a significant step in understanding the formation of hybridization zones due to range expansion potentially associated with climate change.

Genomic basis of melanin-associated phenotypes suggests colour-specific environmental adaptations in tawny owls.

Feathers comprise a series of evolutionary innovations but also harbour colour, a key biological trait known to co-vary with life history or complex traits. Those relationships are particularly true in melanin-based pigmentation species due to known pleiotropic effects of the melanocortin pathway - originating from melanin-associated phenotypes. Here, we explore the molecular basis of melanin colouration and expected co-variation at the molecular level in the melanin-based, colour polymorphic system of the tawny owl (Strix aluco). An extensive body of literature has revealed that grey and brown tawny owl colour morphs differ in a series of life history and behavioural traits. Thus, it is plausible to expect co-variation also at molecular level between colour morphs. To investigate this possibility, we assembled the first draft genome of the species against which we mapped ddRADseq reads from 220 grey and 150 brown morphs - representing 10 years of pedigree data from a population in Southern Finland - and explored genome-wide associations with colour phenotype. Our results revealed putative molecular signatures of cold adaptation strongly associated with the grey phenotype, namely, a non-synonymous substitution in MCHR1, plus 2 substitutions in non-coding regions of FTCD and FAM135A whose genotype combinations obtained a predictive power of up to 100% (predicting grey colour). These suggest a molecular basis of cold environment adaptations predicted to be grey-morph specific. Our results potentially reveal part of the molecular machinery of melanin-associated phenotypes and provide novel insights towards understanding the functional genomics of colour polymorphism in melanin-based pigmented species.

Seascape genomics reveals limited dispersal and suggests spatially varying selection among European populations of sea lamprey (Petromyzon marinus).

Sea lamprey Petromyzon marinus is an anadromous and semelparous fish without homing behaviors. Despite being a freshwater, free-living organism for a large part of their life cycle, its adulthood is spent as a parasite of marine vertebrates. In their native European range, while it is well-established that sea lampreys comprise a single nearly-panmictic population, few studies have further explored the evolutionary history of natural populations. Here, we performed the first genome-wide characterization of sea lamprey's genetic diversity in their European natural range. The objectives were to investigate the connectivity among river basins and explore evolutionary processes mediating dispersal during the marine phase, with the sequencing of 186 individuals from 8 locations spanning the North Eastern Atlantic coast and the North Sea with double-digest RAD-sequencing, obtaining a total of 30,910 bi-allelic SNPs. Population genetic analyses reinforced the existence of a single metapopulation encompassing freshwater spawning sites within the North Eastern Atlantic and the North Sea, though the prevalence of private alleles at northern latitudes suggested some limits to the species' dispersal. Seascape genomics suggested a scenario where oxygen concentration and river runoffs impose spatially varying selection across their distribution range. Exploring associations with the abundance of potential hosts further suggested that hake and cod could also impose selective pressures, although the nature of such putative biotic interactions was unresolved. Overall, the identification of adaptive seascapes in a panmictic anadromous species could contribute to conservation practices by providing information for restoration activities to mitigate local extinctions on freshwater sites.

Bringing to light nuclear-mitochondrial insertions in the genomes of nocturnal predatory birds.

Mito-nuclear insertions, or NUMTs, relate to genetic material of mitochondrial origin that have been transferred to the nuclear DNA molecule. The increasing amounts of genomic data currently being produced presents an opportunity to investigate this type of patterns in genome evolution of non-model organisms. Identifying NUMTs across a range of closely related taxa allows one to generalize patterns of insertion and maintenance in autosomes, which is ultimately relevant to the understanding of genome biology and evolution. Here we collected existing pairwise genome-mitogenome data of the order Strigiformes, a group that includes all the nocturnal bird predators. We identified NUMTs by applying percent similarity thresholds after blasting mitochondrial genomes against nuclear genome assemblies. We identified NUMTsin all genomes with numbers ranging from 4 in Bubo bubo to 24 in Ciccaba nigrolineata. Statistical analyses revealed NUMT size to negatively correlate with NUMT's sequence similarity to with original mtDNA region. Lastly, characterizing these nuclear insertions of mitochondrial origin in a comparative genomics framework produced variable phylogenetic patterns, suggesting in some cases that insertions might pre-date speciation events within Strigiformes.

A noninvasive eDNA tool for detecting sea lamprey larvae in river sediments: Analytical validation and field testing in a low-abundance ecosystem.

Anthropogenic activities are increasingly threatening aquatic biodiversity, especially anadromous species. Monitoring and conservation measures are thus required to protect, maintain and restore imperilled populations. While many species can be surveyed using traditional capture and visual census techniques, species that use riverine habitats in a less conspicuous manner, such as sea lamprey Petromyzon marinus, can be more challenging to monitor. Sea lamprey larvae (ammocoetes) can spend several years in freshwater burrowed within soft sediments, inhibiting their detection and assessment. Here, we present a qPCR assay based on the detection of environmental DNA (eDNA) to identify the presence of ammocoetes burrowed in the sediment. We present an extensively validated method that ensured both species-specificity of the assay as well as the capacity to detect ammocoetes when abundances are low. Experiments on burrowing activity suggested that most of the DNA released into the sediment occurs during burrowing. Overall, we demonstrate this new molecular-based tool is an efficient and effective complement to traditional monitoring activities targeting larval stages of sea lampreys.

Forecasting shifts in habitat suitability across the distribution range of a temperate small pelagic fish under different scenarios of climate change.

Climate change often leads to shifts in the distribution of small pelagic fish, likely by changing the match-mismatch dynamics between these sensitive species within their environmental optima. Using present-day habitat suitability, we projected how different scenarios of climate change (IPCC Representative Concentration Pathways 2.6, 4.5 and 8.5) may alter the large scale distribution of European sardine Sardina pilchardus (a model species) by 2050 and 2100. We evaluated the variability of species-specific environmental optima allowing a comparison between present-day and future scenarios. Regardless of the scenario, sea surface temperature and salinity and the interaction between current velocity and distance to the nearest coast were the main descriptors responsible for the main effects on sardine's distribution. Present-day and future potential "hotspots" for sardine were neritic zones (<250 km) with water currents <0.4 m s-1, where SST was between 10 and 22 °C and SSS > 20 (PSU), on average. Most variability in projected shifts among climatic scenarios was in habitats with moderate to low suitability. By the end of this century, habitat suitability was projected to increase in the Canary Islands, Iberian Peninsula, central North Sea, northern Mediterranean, and eastern Black Sea and to decrease in the Atlantic African coast, southwest Mediterranean, English Channel, northern North Sea and Western U.K. A gradual poleward-eastward shift in sardine distribution was also projected among scenarios. This shift was most pronounced in 2100 under RCP 8.5. In that scenario, sardines had a 9.6% range expansion which included waters along the entire coast of Norway up and into the White Sea. As habitat suitability is mediated by the synergic effects of climate variability and change on species fitness, it is critical to apply models with robust underlying species-habitat data that integrate knowledge on the full range of processes shaping species productivity and distribution.

Targeted Sequencing of Mitochondrial Genes Reveals Signatures of Molecular Adaptation in a Nearly Panmictic Small Pelagic Fish Species.

Ongoing climatic changes, with predictable impacts on marine environmental conditions, are expected to trigger organismal responses. Recent evidence shows that, in some marine species, variation in mitochondrial genes involved in the aerobic conversion of oxygen into ATP at the cellular level correlate with gradients of sea surface temperature and gradients of dissolved oxygen. Here, we investigated the adaptive potential of the European sardine Sardina pilchardus populations offshore the Iberian Peninsula. We performed a seascape genetics approach that consisted of the high throughput sequencing of mitochondria's ATP6, COI, CYTB and ND5 and five microsatellite loci on 96 individuals coupled with environmental information on sea surface temperature and dissolved oxygen across five sampling locations. Results show that, despite sardines forming a nearly panmictic population around Iberian Peninsula, haplotype frequency distribution can be explained by gradients of minimum sea surface temperature and dissolved oxygen. We further identified that the frequencies of the most common CYTB and ATP6 haplotypes negatively correlate with minimum sea surface temperature across the sampled area, suggestive of a signature of selection. With signatures of selection superimposed on highly connected populations, sardines may be able to follow environmental optima and shift their distribution northwards as a response to the increasing sea surface temperatures.

Distribution of genetic diversity reveals colonization patterns and philopatry of the loggerhead sea turtles across geographic scales.

Understanding the processes that underlie the current distribution of genetic diversity in endangered species is a goal of modern conservation biology. Specifically, the role of colonization and dispersal events throughout a species' evolutionary history often remains elusive. The loggerhead sea turtle (Caretta caretta) faces multiple conservation challenges due to its migratory nature and philopatric behaviour. Here, using 4207 mtDNA sequences, we analysed the colonisation patterns and distribution of genetic diversity within a major ocean basin (the Atlantic), a regional rookery (Cabo Verde Archipelago) and a local island (Island of Boa Vista, Cabo Verde). Data analysis using hypothesis-driven population genetic models suggests the colonization of the Atlantic has occurred in two distinct waves, each corresponding to a major mtDNA lineage. We propose the oldest lineage entered the basin via the isthmus of Panama and sequentially established aggregations in Brazil, Cabo Verde and in the area of USA and Mexico. The second lineage entered the Atlantic via the Cape of Good Hope, establishing colonies in the Mediterranean Sea, and from then on, re-colonized the already existing rookeries of the Atlantic. At the Cabo Verde level, we reveal an asymmetric gene flow maintaining links across island-specific nesting groups, despite significant genetic structure. This structure stems from female philopatric behaviours, which could further be detected by weak but significant differentiation amongst beaches separated by only a few kilometres on the island of Boa Vista. Exploring biogeographic processes at diverse geographic scales improves our understanding of the complex evolutionary history of highly migratory philopatric species. Unveiling the past facilitates the design of conservation programmes targeting the right management scale to maintain a species' evolutionary potential.

Genomic footprints of a biological invasion: Introduction from Asia and dispersal in Europe of the topmouth gudgeon (Pseudorasbora parva).

Facilitated by the intensification of global trading, the introduction and dispersal of species to areas in which they are historically non-native is nowadays common. From an evolutionary standpoint, invasions are paradoxical: not only non-native environments could be different from native ones for which introduced individuals would be ill-adapted, but also small founding population size should be associated with reduced adaptive potential. As such, biological invasions are considered valuable real-time evolutionary experiments. Here, we investigated the population structure and adaptive potential of the highly invasive topmouth gudgeon (Pseudorasbora parva) across Europe and East Asia. We RAD-sequenced 301 specimens from sixteen populations and three distinct within-catchment invaded regions as well as two locations in the native range. With 13,785 single nucleotide polymorphisms, we provide conclusive evidence for a genome-wide signature of two distinct invasion events, in Slovakia and Turkey, each originating from a specific area in the native range. A third invaded area, in France, appears to be the result of dispersal within the invasive range. Few loci showed signs of selection, the vast majority of which being identified in the Slovakian region. Functional annotation suggests that faster early stage development, resistance to pollution and immunocompetence contribute to the invasion success of the local habitats. By showing that populations in the invasive range have different evolutionary histories, our study reinforces the idea that populations, rather than species, are the units to consider in invasion biology.

Conservation of genetic uniqueness in remaining populations of red squirrels (Sciurus vulgaris L.) in the South of England.

The Eurasian red squirrel (Sciurus vulgaris) is an emblematic species for conservation, and its decline in the British Isles exemplifies the impact that alien introductions can have on native ecosystems. Indeed, red squirrels in this region have declined dramatically over the last 60 years due to the spread of squirrelpox virus following the introduction of the gray squirrel (Sciurus carolinensis). Currently, red squirrel populations in Britain are fragmented and need to be closely monitored in order to assess their viability and the effectiveness of conservation efforts. The situation is even more dramatic in the South of England, where S. vulgaris survives only on islands (Brownsea Island, Furzey Island, and the Isle of Wight). Using the D-loop, we investigated the genetic diversity and putative ancestry of the squirrels from Southern England and compared them to a European dataset composed of 1,016 samples from 54 populations. We found that our three populations were more closely related to other squirrels from the British Isles than squirrels from Europe, showed low genetic diversity, and also harbored several private haplotypes. Our study demonstrates how genetically unique the Southern English populations are in comparison with squirrels from the continental European range. We report the presence of four private haplotypes, suggesting that these populations may potentially harbor distinct genetic lineages. Our results emphasize the importance of preserving these isolated red squirrel populations for the conservation of the species.

Is salinity an obstacle for biological invasions?

Invasions of freshwater habitats by marine and brackish species have become more frequent in recent years with many of those species originating from the Ponto-Caspian region. Populations of Ponto-Caspian species have successfully established in the North and Baltic Seas and their adjoining rivers, as well as in the Great Lakes-St. Lawrence River region. To determine if Ponto-Caspian taxa more readily acclimatize to and colonize diverse salinity habitats than taxa from other regions, we conducted laboratory experiments on 22 populations of eight gammarid species native to the Ponto-Caspian, Northern European and Great Lakes-St. Lawrence River regions. In addition, we conducted a literature search to survey salinity ranges of these species worldwide. Finally, to explore evolutionary relationships among examined species and their populations, we sequenced the mitochondrial cytochrome c oxidase subunit I gene (COI) from individuals used for our experiments. Our study revealed that all tested populations tolerate wide ranges of salinity, however, different patterns arose among species from different regions. Ponto-Caspian taxa showed lower mortality in fresh water, while Northern European taxa showed lower mortality in fully marine conditions. Genetic analyses showed evolutionary divergence among species from different regions. Due to the geological history of the two regions, as well as high tolerance of Ponto-Caspian species to fresh water, whereas Northern European species are more tolerant of fully marine conditions, we suggest that species originating from the Ponto-Caspian and Northern European regions may be adapted to freshwater and marine environments, respectively. Consequently, the perception that Ponto-Caspian species are more successful colonizers might be biased by the fact that areas with highest introduction frequency of NIS (i.e., shipping ports) are environmentally variable habitats which often include freshwater conditions that cannot be tolerated by euryhaline taxa of marine origin.

Diversity and distribution of genetic variation in gammarids: Comparing patterns between invasive and non-invasive species.

Biological invasions are worldwide phenomena that have reached alarming levels among aquatic species. There are key challenges to understand the factors behind invasion propensity of non-native populations in invasion biology. Interestingly, interpretations cannot be expanded to higher taxonomic levels due to the fact that in the same genus, there are species that are notorious invaders and those that never spread outside their native range. Such variation in invasion propensity offers the possibility to explore, at fine-scale taxonomic level, the existence of specific characteristics that might predict the variability in invasion success. In this work, we explored this possibility from a molecular perspective. The objective was to provide a better understanding of the genetic diversity distribution in the native range of species that exhibit contrasting invasive propensities. For this purpose, we used a total of 784 sequences of the cytochrome c oxidase subunit I of mitochondrial DNA (mtDNA-COI) collected from seven Gammaroidea, a superfamily of Amphipoda that includes species that are both successful invaders (Gammarus tigrinus, Pontogammarus maeoticus, and Obesogammarus crassus) and strictly restricted to their native regions (Gammarus locusta, Gammarus salinus, Gammarus zaddachi, and Gammarus oceanicus). Despite that genetic diversity did not differ between invasive and non-invasive species, we observed that populations of non-invasive species showed a higher degree of genetic differentiation. Furthermore, we found that both geographic and evolutionary distances might explain genetic differentiation in both non-native and native ranges. This suggests that the lack of population genetic structure may facilitate the distribution of mutations that despite arising in the native range may be beneficial in invasive ranges. The fact that evolutionary distances explained genetic differentiation more often than geographic distances points toward that deep lineage divergence holds an important role in the distribution of neutral genetic diversity.

Animal Navigation: The Eel's Magnetic Guide to the Gulf Stream.

The geographic distribution of migratory species can span thousands of kilometers. Yet, traits that enable large-scale migrations are poorly understood. A recent study demonstrates that juvenile eels use the Earth's magnetism for their dispersal, with possible implications for their evolution.

Does asymmetric gene flow among matrilines maintain the evolutionary potential of the European eel?

Using evolutionary theory to predict the dynamics of populations is one of the aims of evolutionary conservation. In endangered species, with geographic range extending over continuous areas, the predictive capacity of evolutionary-based conservation measures greatly depends on the accurate identification of reproductive units. The endangered European eel (Anguilla anguilla) is a highly migratory fish species with declining population due to a steep recruitment collapse in the beginning of the 1980s. Despite punctual observations of genetic structure, the population is viewed as a single panmictic reproductive unit. To understand the possible origin of the detected structure in this species, we used a combination of mitochondrial and nuclear loci to indirectly evaluate the possible existence of cryptic demes. For that, 403 glass eels from three successive cohorts arriving at a single location were screened for phenotypic and genetic diversity, while controlling for possible geographic variation. Over the 3 years of sampling, we consistently identified three major matrilines which we hypothesized to represent demes. Interestingly, not only we found that population genetic models support the existence of those matriline-driven demes over a completely panmictic mode of reproduction, but also we found evidence for asymmetric gene flow amongst those demes. We uphold the suggestion that the detection of demes related to those matrilines reflect a fragmented spawning ground, a conceptually plausible consequence of the low abundance that the European eel has been experiencing for three decades. Furthermore, we suggest that this cryptic organization may contribute to the maintenance of the adaptive potential of the species.

Evaluating the adaptive potential of the European eel: is the immunogenetic status recovering?

The recent increased integration of evolutionary theory into conservation programs has greatly improved our ability to protect endangered species. A common application of such theory links population dynamics and indices of genetic diversity, usually estimated from neutrally evolving markers. However, some studies have suggested that highly polymorphic adaptive genes, such as the immune genes of the Major Histocompatibility Complex (MHC), might be more sensitive to fluctuations in population dynamics. As such, the combination of neutrally- and adaptively-evolving genes may be informative in populations where reductions in abundance have been documented. The European eel (Anguilla anguilla) underwent a drastic and well-reported decline in abundance in the late 20th century and still displays low recruitment. Here we compared genetic diversity indices estimated from neutral (mitochondrial DNA and microsatellites) and adaptive markers (MHC) between two distinct generations of European eels. Our results revealed a clear discrepancy between signatures obtained for each class of markers. Although mtDNA and microsatellites showed no changes in diversity between the older and the younger generations, MHC diversity revealed a contemporary drop followed by a recent increase. Our results suggest ongoing gain of MHC genetic diversity resulting from the interplay between drift and selection and ultimately increasing the adaptive potential of the species.

Recruitment collapse and population structure of the European eel shaped by local ocean current dynamics.

Worldwide, exploited marine fish stocks are under threat of collapse [1]. Although the drivers behind such collapses are diverse, it is becoming evident that failure to consider evolutionary processes in fisheries management can have drastic consequences on a species' long-term viability [2]. The European eel (Anguilla anguilla; Linnaeus, 1758) is no exception: not only does the steep decline in recruitment observed in the 1980s [3, 4] remain largely unexplained, the punctual detection of genetic structure also raises questions regarding the existence of a single panmictic population [5-7]. With its extended Transatlantic dispersal, pinpointing the role of ocean dynamics is crucial to understand both the population structure and the widespread decline of this species. Hence, we combined dispersal simulations using a half century of high-resolution ocean model data with population genetics tools. We show that regional atmospherically driven ocean current variations in the Sargasso Sea were the major driver of the onset of the sharp decline in eel recruitment in the beginning of the 1980s. The simulations combined with genotyping of natural coastal eel populations furthermore suggest that unexpected evidence of coastal genetic differentiation is consistent with cryptic female philopatric behavior within the Sargasso Sea. Such results demonstrate the key constraint of the variable oceanic environment on the European eel population.