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The contemporary diversity and distribution of species are shaped by their evolutionary and ecological history. This can be deciphered with the help of phylogenetic and demographic analysis methods, ideally combining and supplementing information from mitochondrial and nuclear genomes. In this study, we investigated the demographic history of Eurasian perch (Perca fluviatilis), a highly adaptable teleost with a distribution range across Eurasia. We combined whole-genome resequencing data with available genomic resources to analyse the phylogeny, phylogeography, and demographic history of P. fluviatilis populations from Europe and Siberia. We identified five highly diverged evolutionary mtDNA lineages, three of which show a strong signal of admixture in the Baltic Sea region. The estimated mean divergence time between these lineages ranged from 0.24 to 1.42 million years. Based on nuclear genomes, two distinct demographic trajectories were observed in European and Siberian samples reflecting contrasting demographic histories ca. 30,000-100,000 years before the present. A comparison of mtDNA and nuclear DNA evolutionary trees and AMOVA revealed concordances, as well as incongruences, between the two types of data, most likely reflecting recent postglacial colonization and hybridization events. Overall, our findings demonstrate the power and usefulness of genome-wide information for delineating historical processes that have shaped the genome of P. fluviatilis. We also highlight the added value of data-mining existing transcriptomic resources to complement novel sequence data, helping to shed light on putative glacial refugia and postglacial recolonization routes.
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Extreme environments are inhospitable to the majority of species, but some organisms are able to survive in such hostile conditions due to evolutionary adaptations. For example, modern bony fishes have colonized various aquatic environments, including perpetually dark, hypoxic, hypersaline and toxic habitats. Eurasian perch (Perca fluviatilis) is among the few fish species of northern latitudes that is able to live in very acidic humic lakes. Such lakes represent almost "nocturnal" environments; they contain high levels of dissolved organic matter, which in addition to creating a challenging visual environment, also affects a large number of other habitat parameters and biotic interactions. To reveal the genomic targets of humic-associated selection, we performed whole-genome sequencing of perch originating from 16 humic and 16 clear-water lakes in northern Europe. We identified over 800,000 single nucleotide polymorphisms, of which >10,000 were identified as potential candidates under selection (associated with >3000 genes) using multiple outlier approaches. Our findings suggest that adaptation to the humic environment may involve hundreds of regions scattered across the genome. Putative signals of adaptation were detected in genes and gene families with diverse functions, including organism development and ion transportation. The observed excess of variants under selection in regulatory regions highlights the importance of adaptive evolution via regulatory elements, rather than via protein sequence modification. Our study demonstrates the power of whole-genome analysis to illuminate the multifaceted nature of humic adaptation and provides the foundation for further investigation of causal mutations underlying phenotypic traits of ecological and evolutionary importance.
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Percas , Animales , Ecosistema , Genoma/genética , Sustancias Húmicas , Lagos , Percas/genéticaRESUMEN
Parental age can affect offspring telomere length through heritable and epigenetic-like effects, but at what stage during development these effects are established is not well known. To address this, we conducted a cross-fostering experiment in common gulls (Larus canus) that enabled us distinguish between pre- and post-natal parental age effects on offspring telomere length. Whole clutches were exchanged after clutch completion within and between parental age classes (young and old) and blood samples were collected from chicks at hatching and during the fastest growth phase (11 days later) to measure telomeres. Neither the ages of the natal nor the foster parents predicted the telomere length or the change in telomere lengths of their chicks. Telomere length (TL) was repeatable within chicks, but increased across development (repeatability = 0.55, intraclass correlation coefficient within sampling events 0.934). Telomere length and the change in telomere length were not predicted by post-natal growth rate. Taken together, these findings suggest that in common gulls, telomere length during early life is not influenced by parental age or growth rate, which may indicate that protective mechanisms buffer telomeres from external conditions during development in this relatively long-lived species.
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Charadriiformes , Animales , Charadriiformes/genética , Acortamiento del Telómero/genética , Telómero/genéticaRESUMEN
Maternal effects affect offspring phenotype and fitness. However, the roles of offspring sex-specific sensitivity to maternal glucocorticoids and sex-biased maternal investment remain unclear. It is also uncertain whether telomere length (a marker associated with lifespan) depends on early growth in a sex-specific manner. We assessed whether maternal traits including corticosterone (CORT; the main avian glucocorticoid) and in ovo growth rate are sex-specifically related to offspring CORT exposure, relative telomere length (RTL) and body condition in eiders (Somateria mollissima). We measured feather CORT (fCORT), RTL and body condition of newly hatched ducklings, and growth rate in ovo was expressed as tarsus length at hatching per incubation duration. Maternal traits included baseline plasma CORT, RTL, body condition and breeding experience. We found that fCORT was negatively associated with growth rate in daughters, while it showed a positive association in sons. Lower offspring fCORT was associated with higher maternal baseline plasma CORT, and fCORT was higher in larger clutches and in those hatching later. The RTL of daughters was negatively associated with maternal RTL, whereas that of males was nearly independent of maternal RTL. Higher fCORT in ovo was associated with longer RTL at hatching in both sexes. Duckling body condition was mainly explained by egg weight, and sons had a slightly lower body condition. Our correlational results suggest that maternal effects may have heterogeneous and even diametrically opposed effects between the sexes during early development. Our findings also challenge the view that prenatal CORT exposure is invariably associated with shorter telomeres.
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Corticosterona , Patos , Animales , Cruzamiento , Femenino , Glucocorticoides , Masculino , FenotipoRESUMEN
Snapshot analyses have demonstrated dramatic intraspecific variation in the degree of brain sexual size dimorphism (SSD). Although brain SSD is believed to be generated by the sex-specific cognitive demands of reproduction, the relative roles of developmental and population-specific contributions to variation in brain SSD remain little studied. Using a common garden experiment, we tested for sex-specific changes in brain anatomy over the breeding cycle in three-spined stickleback (Gasterosteus aculeatus) sampled from four locations in northern Europe. We found that the male brain increased in size (ca. 24%) significantly more than the female brain towards breeding, and that the resulting brain SSD was similar (ca. 20%) for all populations over the breeding cycle. Our findings support the notion that the stickleback brain is highly plastic and changes over the breeding cycle, especially in males, likely as an adaptive response to the cognitive demands of reproduction (e.g. nest construction and parental care). The results also provide evidence to suggest that breeding-related changes in brain size may be the reason for the widely varying estimates of brain SSD across studies of this species, cautioning against interpreting brain size measurements from a single time point as fixed/static.
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Tamaño de los Órganos/fisiología , Caracteres Sexuales , Smegmamorpha/fisiología , Adaptación Fisiológica , Animales , Europa (Continente) , Femenino , Masculino , Reproducción/fisiología , Smegmamorpha/anatomía & histologíaRESUMEN
In order to assess the accuracy and reliability of age estimates from calcified structures in the three-spined stickleback Gasterosteus aculeatus, we evaluated intra and inter-reader repeatability from three structures: otoliths, gill covers and pelvic spines). Average age estimates were also compared between the structures. The overall intra-reader repeatability of age estimates were highest for otoliths (69%), lowest for gill covers (53%) and intermediate for spine cross-sections (63%). Although four of the seven readers had the highest intra-reader repeatability score for spine cross-sections, the inter-reader variance in this structure was much higher than in others. Otoliths were the easiest in terms of their pre-analysis treatment and exchange of materials (as digital images) between readers. In addition, otoliths are more well-studied compared with the other structures with respect to their development through ontogenesis; hence, age estimates based on otoliths should be the most reliable. Therefore, our recommendation is that whenever possible, analysis of otoliths should be the preferred approach for aging G. aculeatus.
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Branquias/anatomía & histología , Membrana Otolítica/anatomía & histología , Smegmamorpha/crecimiento & desarrollo , Animales , Reproducibilidad de los Resultados , Smegmamorpha/anatomía & histologíaRESUMEN
Telomeres are highly conserved nucleoprotein structures which protect genome integrity. The length of telomeres is influenced by both genetic and environmental factors, but relatively little is known about how different hereditary and environmental factors interact in determining telomere length. We manipulated growth rates and timing of maturation by exposing full-sib nine-spined sticklebacks (Pungitius pungitius) to two different temperature treatments and quantified the effects of temperature treatments, sex, timing of maturation, growth rate and family (genetic influences) on telomere length. We did not find the overall effect of temperature treatment on the relative telomere length. However, we found that variation in telomere length was related to timing of maturation in a sex- and temperature-dependent manner. Telomere length was negatively related to age at maturation in elevated temperature and early maturing males and females differed in telomere length. Variation in growth rate did not explain any variation in telomere length. The broad sense heritability (h 2) of telomere length was estimated at h 2 = 0.31 - 0.47, suggesting predominance of environmental over genetic determinants of telomere length variability. This study provides the first evidence that age at maturation together with factors associated with it are influencing telomere length in an ectotherm. Future studies are encouraged to identify the extent to which these results can be replicated in other ectotherms.
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Peces , Telómero , Animales , Femenino , Peces/genética , Masculino , Smegmamorpha , TemperaturaRESUMEN
Life-history theory predicts that organisms optimize their resource allocation strategy to maximize lifetime reproductive success. Individuals can flexibly reallocate resources depending on their life-history stage, and environmental and physiological factors, which lead to variable life-history strategies even within species. Physiological trade-offs between immunity and reproduction are particularly relevant for long-lived species that need to balance current reproduction against future survival and reproduction, but their underlying mechanisms are poorly understood. A major unresolved issue is whether the first-line innate immune function is suppressed by reproductive investment. In this paper, we tested if reproductive investment is associated with the suppression of innate immunity, and how this potential trade-off is resolved depending on physiological state and residual reproductive value. We used long-lived capital-breeding female eiders (Somateria mollissima) as a model. We showed that the innate immune response, measured by plasma bacteria-killing capacity (BKC), was negatively associated with increasing reproductive investment, i.e., with increasing clutch size and advancing incubation stage. Females in a better physiological state, as indexed by low heterophil-to-lymphocyte (H/L) ratios, showed higher BKC during early incubation, but this capacity decreased as incubation progressed, whereas females in poorer state showed low BKC capacity throughout incubation. Although plasma BKC generally declined with increasing H/L ratios, this decrease was most pronounced in young females. Our results demonstrate that reproductive investment can suppress constitutive first-line immune defence in a long-lived bird, but the degree of immunosuppression depends on physiological state and age.
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Reproducción , Animales , Anseriformes , Aves/inmunología , Inmunidad InnataRESUMEN
The mosaic model of brain evolution postulates that different brain regions are relatively free to evolve independently from each other. Such independent evolution is possible only if genetic correlations among the different brain regions are less than unity. We estimated heritabilities, evolvabilities and genetic correlations of relative size of the brain, and its different regions in the three-spined stickleback (Gasterosteus aculeatus). We found that heritabilities were low (average h(2) = 0.24), suggesting a large plastic component to brain architecture. However, evolvabilities of different brain parts were moderate, suggesting the presence of additive genetic variance to sustain a response to selection in the long term. Genetic correlations among different brain regions were low (average rG = 0.40) and significantly less than unity. These results, along with those from analyses of phenotypic and genetic integration, indicate a high degree of independence between different brain regions, suggesting that responses to selection are unlikely to be severely constrained by genetic and phenotypic correlations. Hence, the results give strong support for the mosaic model of brain evolution. However, the genetic correlation between brain and body size was high (rG = 0.89), suggesting a constraint for independent evolution of brain and body size in sticklebacks.
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Evolución Biológica , Encéfalo/anatomía & histología , Variación Genética , Smegmamorpha/anatomía & histología , Smegmamorpha/genética , Animales , Femenino , Masculino , Tamaño de los ÓrganosRESUMEN
BACKGROUND: Plasticity in brain size and the size of different brain regions during early ontogeny is known from many vertebrate taxa, but less is known about plasticity in the brains of adults. In contrast to mammals and birds, most parts of a fish's brain continue to undergo neurogenesis throughout adulthood, making lifelong plasticity in brain size possible. We tested whether maturing adult three-spined sticklebacks (Gasterosteus aculeatus) reared in a stimulus-poor environment exhibited brain plasticity in response to environmental enrichment, and whether these responses were sex-specific, thus altering the degree of sexual size dimorphism in the brain. RESULTS: Relative sizes of total brain and bulbus olfactorius showed sex-specific responses to treatment: males developed larger brains but smaller bulbi olfactorii than females in the enriched treatment. Hence, the degree of sexual size dimorphism (SSD) in relative brain size and the relative size of the bulbus olfactorius was found to be environment-dependent. Furthermore, the enriched treatment induced development of smaller tecta optica in both sexes. CONCLUSIONS: These results demonstrate that adult fish can alter the size of their brain (or brain regions) in response to environmental stimuli, and these responses can be sex-specific. Hence, the degree of SSD in brain size can be environment-dependent, and our results hint at the possibility of a large plastic component to SSD in stickleback brains. Apart from contributing to our understanding of the processes shaping and explaining variation in brain size and the size of different brain regions in the wild, the results show that provision of structural complexity in captive environments can influence brain development. Assuming that the observed plasticity influences fish behaviour, these findings may also have relevance for fish stocking, both for economical and conservational purposes.
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Eye flukes (Diplostomidae) are diverse and abundant trematode parasites that form multi-species communities in fish with negative effects on host fitness and survival. However, the environmental factors and host-related characteristics that determine species diversity, composition, and coexistence in such communities remain poorly understood. Here, we developed a cost-effective cox1 region-specific DNA metabarcoding approach to characterize parasitic diplostomid communities in two common fish species (Eurasian perch and common roach) collected from seven temperate lakes in Estonia. We found considerable inter- and intra-lake, as well as inter-host species, variation in diplostomid communities. Sympatric host species characterization revealed that parasite communities were typically more diverse in roach than perch. Additionally, we detected five positive and two negative diplostomid species associations in roach, whereas only a single negative association was observed in perch. These results indicate that diplostomid communities in temperate lakes are complex and dynamic systems exhibiting both spatial and temporal heterogeneity. They are influenced by various environmental factors and by host-parasite and inter-parasite interactions. We expect that the described methodology facilitates ecological and biodiversity research of diplostomid parasites. It is also adaptable to other parasite groups where it could serve to improve current understanding of diversity, distribution, and interspecies interactions of other understudied taxa.
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Cyprinidae , Enfermedades de los Peces , Parásitos , Percas , Trematodos , Animales , Lagos/parasitología , Ecosistema , Código de Barras del ADN Taxonómico , Percas/parasitología , Cyprinidae/parasitología , Trematodos/genética , Enfermedades de los Peces/parasitologíaRESUMEN
Determining the physiological effects of parasites and characterizing genes involved in host responses to infections are essential to improving our understanding of host-parasite interactions and their ecological and evolutionary consequences. This task, however, is complicated by high diversity and complex life histories of many parasite species. The use of transcriptomics in the context of wild-caught specimens can help ameliorate this by providing both qualitative and quantitative information on gene expression patterns in response to parasites in specific host organs and tissues. Here, we evaluated the physiological impact of the widespread parasite, the pike tapeworm (Triaenophorus nodulosus), on its second intermediate host, the Eurasian perch (Perca fluviatilis). We used an RNAseq approach to analyse gene expression in the liver, the target organ of T. nodulosus plerocercoids, and spleen which is one of the main immune organs in teleost fishes. We compared perch collected from multiple lakes consisting of individuals with (n = 8) and without (n = 6) T. nodulosus plerocercoids in the liver. Results revealed a small number of differentially expressed genes (DEGs, adjusted p-value ≤0.05) in both spleen (n = 22) and liver (n = 10). DEGs in spleen consisted of mostly upregulated immune related genes (e.g., JUN, SIK1, THSB1), while those in the liver were often linked to metabolic functions (e.g., FABP1, CADM4, CDAB). However, Gene Ontology (GO) analysis showed lack of functional enrichment among DEGs. This study demonstrates that Eurasian perch displays a subtle response at a gene expression level to T. nodulosus plerocercoid infection. Given that plerocercoids are low-metabolic activity transmission stages, our results suggest that moderate T. nodulosus plerocercoid infection most likely does not provoke an extensive host immune response and have relatively low physiological costs for the host. Our findings illustrate that not all conspicuous infections have severe effects on host gene regulation.
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Intra-group relatedness does not necessarily imply kin selection, a leading explanation for social evolution. An overlooked mechanism for generating population genetic structure is variation in longevity and fecundity, referred to as individual quality, affecting kin structure and the potential for cooperation. Individual quality also affects choosiness in partner choice, a key process explaining cooperation through direct fitness benefits. Reproductive skew theory predicts that relatedness decreases with increasing group size, but this relationship could also arise because of quality-dependent demography and partner choice, without active kin association. We addressed whether brood-rearing eider (Somateria mollissima) females preferentially associated with kin using a 6-year data set with individuals genotyped at 19 microsatellite loci and tested whether relatedness decreased with increasing female group size. We also determined the relationship between local relatedness and indices of female age and body condition. We further examined whether the level of female intracoalition relatedness differed from background relatedness in any year. As predicted, median female intra-group relatedness decreased with increasing female group size. However, the proportion of related individuals increased with advancing female age, and older females prefer smaller brood-rearing coalitions, potentially producing a negative relationship between group size and relatedness. There were considerable annual fluctuations in the level of relatedness between coalition-forming females, and in 1year this level exceeded that expected by random association. Thus, both passive and active mechanisms govern kin associations in brood-rearing eiders. Eiders apparently can discriminate between kin, but the benefits of doing so may vary over time.
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Anseriformes/genética , Genética de Población , Comportamiento de Nidificación , Conducta Social , Animales , Anseriformes/fisiología , Femenino , Genotipo , Repeticiones de Microsatélite , Densidad de Población , Análisis de Secuencia de ADNRESUMEN
The wels catfish (Silurus glanis) is one of the largest freshwater fish species in the world. This top predator plays a key role in ecosystem stability, and represents an iconic trophy-fish for recreational fishermen. S. glanis is also a highly valued species for its high-quality boneless flesh, and has been cultivated for over 100 years in Eastern and Central Europe. The interest in rearing S. glanis continues to grow; the aquaculture production of this species has almost doubled during the last decade. However, despite its high ecological, cultural and economic importance, the available genomic resources for S. glanis are very limited. To fulfill this gap we report a de novo assembly and annotation of the whole genome sequence of a female S. glanis The linked-read based technology with 10X Genomics Chromium chemistry and Supernova assembler produced a highly continuous draft genome of S. glanis: â¼0.8Gb assembly (scaffold N50 = 3.2 Mb; longest individual scaffold = 13.9 Mb; BUSCO completeness = 84.2%), which included 313.3 Mb of putative repeated sequences. In total, 21,316 protein-coding genes were predicted, of which 96% were annotated functionally from either sequence homology or protein signature searches. The highly continuous genome assembly will be an invaluable resource for aquaculture genomics, genetics, conservation, and breeding research of S. glanis.
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Bagres , Ecosistema , Animales , Bagres/genética , Europa (Continente) , Femenino , Agua Dulce , GenomaRESUMEN
BACKGROUND: Next generation sequencing (NGS) technologies are extensively used to dissect the molecular mechanisms of host-parasite interactions in human pathogens. However, ecological studies have yet to fully exploit the power of NGS as a rich source for formulating and testing new hypotheses. METHODS: We studied Eurasian perch (Perca fluviatilis) and its eye parasite (Trematoda, Diplostomidae) communities in 14 lakes that differed in humic content in order to explore host-parasite-environment interactions. We hypothesised that high humic content along with low pH would decrease the abundance of the intermediate hosts (gastropods), thus limiting the occurrence of diplostomid parasites in humic lakes. This hypothesis was initially invoked by whole eye RNA-seq data analysis and subsequently tested using PCR-based detection and a novel targeted metabarcoding approach. RESULTS: Whole eye transcriptome results revealed overexpression of immune-related genes and the presence of eye parasite sequences in RNA-seq data obtained from perch living in clear-water lakes. Both PCR-based and targeted-metabarcoding approach showed that perch from humic lakes were completely free from diplostomid parasites, while the prevalence of eye flukes in clear-water lakes that contain low amounts of humic substances was close to 100%, with the majority of NGS reads assigned to Tylodelphys clavata. CONCLUSIONS: High intraspecific diversity of T. clavata indicates that massively parallel sequencing of naturally pooled samples represents an efficient and powerful strategy for shedding light on cryptic diversity of eye parasites. Our results demonstrate that perch populations in clear-water lakes experience contrasting eye parasite pressure compared to those from humic lakes, which is reflected by prevalent differences in the expression of immune-related genes in the eye. This study highlights the utility of NGS to discover novel host-parasite-environment interactions and provide unprecedented power to characterize the molecular diversity of cryptic parasites.
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Lagos/química , Percas/parasitología , Trematodos/aislamiento & purificación , Animales , ADN de Helmintos , Ojo/parasitología , Enfermedades de los Peces/diagnóstico , Enfermedades de los Peces/parasitología , Interacciones Huésped-Parásitos , Humanos , Sustancias Húmicas , Lagos/parasitología , Reacción en Cadena de la Polimerasa/métodos , RNA-Seq/métodos , Caracoles/parasitología , Trematodos/genética , Infecciones por Trematodos/veterinariaRESUMEN
Evidence for phenotypic plasticity in brain size and the size of different brain parts is widespread, but experimental investigations into this effect remain scarce and are usually conducted using individuals from a single population. As the costs and benefits of plasticity may differ among populations, the extent of brain plasticity may also differ from one population to another. In a common garden experiment conducted with three-spined sticklebacks (Gasterosteus aculeatus) originating from four different populations, we investigated whether environmental enrichment (aquaria provided with structural complexity) caused an increase in the brain size or size of different brain parts compared to controls (bare aquaria). We found no evidence for a positive effect of environmental enrichment on brain size or size of different brain parts in either of the sexes in any of the populations. However, in all populations, males had larger brains than females, and the degree of sexual size dimorphism (SSD) in relative brain size ranged from 5.1 to 11.6% across the populations. Evidence was also found for genetically based differences in relative brain size among populations, as well as for plasticity in the size of different brain parts, as evidenced by consistent size differences among replicate blocks that differed in their temperature.
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Populations are from time to time exposed to stressful temperatures. Their thermal resistance levels are determined by inherent and plastic mechanisms, which are both likely to be under selection in natural populations. Previous studies on Drosophila species have shown that inherent resistance is highly species specific, and differs among ecotypes (e.g., tropical and widespread species). Apart from being exposed to thermal stress many small and fragmented populations face genetic challenges due to, for example, inbreeding. Inbreeding has been shown to reduce inherent resistance levels toward stressful temperatures, but whether adaptation to thermal stress through plastic responses also is affected by inbreeding is so far not clear. In this study, we test inherent cold resistance and the ability to respond plastically to temperature changes through developmental cold acclimation in inbred and outbred lines of five tropical and five widespread Drosophila species. Our results confirm that tropical species have lower cold resistance compared to widespread species, and show that (1) inbreeding reduces inherent cold resistance in both tropical and widespread species, (2) inbreeding does not affect the ability to respond adaptively to temperature acclimation, and (3) tropical species with low basal resistance show stronger adaptive plastic responses to developmental acclimation compared to widespread species.