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Many animals show an aversion to bright, open spaces, with significant variability seen across species, populations and individuals within populations. Although there is much interest in the underlying causes of this behaviour, few studies have been able to systematically isolate the role of heritable and environmental effects. Here, we addressed this gap using a common garden experiment with cavefish. Specifically, we bred and cross-bred cave loaches (Barbatula barbatula), Europe's only known cavefish, in the laboratory, raised the offspring in complete darkness or normal light conditions, and studied their light avoidance behaviour. Cavefish spent much more time in a light area and ventured further out, while surface fish spent considerable time in risk-assessment behaviour between the light and dark areas. Hybrids behaved most similarly to cavefish. Light treatment and eye quality and lens size only had a modest effect. Our results suggest light avoidance behaviour of cavefish has a heritable basis and is fundamentally linked to increased boldness rather than reduced vision, which is likely adaptive given the complete lack of macropredators in the cave environment. Our study provides novel experimental insights into the behavioural divergence of cavefish and contributes to our broader understanding of the evolution of boldness and behavioural adaptation.
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The Aach cave loach (Barbatula barbatula), a recently discovered member of the Nemacheilidae family, offers a unique opportunity to understand the mechanisms underlying evolutionary change. In a common garden experiment, we reared groups of laboratory-bred cave, surface, and hybrid loach under different light conditions. Troglomorphic characters varied significantly among the fish, influenced to a different extent by parental origin and light conditions. Cavefish progeny consistently exhibited smaller eyes, lighter pigmentation, longer barbels, and larger olfactory epithelia than surface fish, while hybrids displayed intermediate characteristics. Surface and hybrid fish raised in complete darkness resembled the cavefish phenotype, while cavefish raised under a natural photoperiod approached the surface form. Characters associated with eye degeneration were found to be primarily heritable. Conversely, traits related to chemo- and mechano-reception were enhanced in the surface and hybrid groups reared in complete darkness, suggesting phenotypic plasticity. Our findings offer valuable insights into the interplay between genetic differentiation and phenotypic plasticity to troglomorphic adaption. This contributes to the broader understanding of the early stages of adaptation, where phenotypic plasticity, drift, and selection shape phenotypes. Relatively recently established cavefish, such as the Aach cave loach, are promising candidates for comparative research investigating evolutionary mechanisms.
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Adaptação Fisiológica , Evolução Biológica , Animais , Adaptação Fisiológica/genética , Peixes , Deriva Genética , Cavernas , OlhoRESUMO
Identification of parasite species is particularly challenging in larval and juvenile hosts, and this hampers the understanding of parasite acquisition in early life. The work described here employs a new combination of methods to identify parasite species and study parasite succession in fry of perch (Perca fluviatilis) from Lake Constance, Germany. Classical morphological diagnostics are combined with sequence comparisons between parasite life-stages collected from various hosts within the same ecosystem. In perch fry at different stages of development, 13 different parasite species were found. Incomplete morphological identifications of cestodes of the order Proteocephalidea, and trematodes of the family Diplostomatidae were complemented with sequences of mitochondrial DNA (cytochrome oxidase 1) and/or nuclear (28 s rDNA) genes. Sequences were compared to published data and used to link the parasites in perch to stages from molluscs, arthropods and more easily identifiable developmental stages from other fishes collected in Lake Constance, which both aided parasite identification and clarified transmission pathways. There were distinct changes in parasite community composition and abundance associated with perch fry age and habitat shifts. Some parasites became more abundant in older fish, whereas the composition of parasite communities was more strongly affected by the ontogenetic shifts from the pelagic to the littoral zone.
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Doenças dos Peixes/parasitologia , Helmintíase Animal/parasitologia , Helmintos/genética , Percas/parasitologia , Animais , Copépodes/classificação , Copépodes/genética , DNA Ribossômico/genética , DNA Espaçador Ribossômico/genética , Ectoparasitoses/parasitologia , Ectoparasitoses/veterinária , Complexo IV da Cadeia de Transporte de Elétrons/genética , Doenças dos Peixes/epidemiologia , Doenças dos Peixes/transmissão , Alemanha/epidemiologia , Helmintíase Animal/epidemiologia , Helmintíase Animal/transmissão , Helmintos/classificação , Interações Hospedeiro-Parasita , Lagos , Filogenia , PrevalênciaRESUMO
Parasitism is ubiquitous in the animal kingdom. Although many fundamental aspects of host-parasite relationships have been unravelled, few studies have systematically investigated how parasites affect organismal movement. Here we combine behavioural experiments of Schistocephalus solidus infected sticklebacks with individual-based simulations to understand how parasitism affects individual movement ability and thereby shapes social interaction patterns. High-resolution tracking revealed that infected fish swam, accelerated, and turned more slowly than did non-infected fish, and tended to be more predictable in their movements. Importantly, the strength of these effects increased with increasing parasite load (proportion of body weight), with more heavily infected fish showing larger changes and impairments in behaviour. When grouped, pairs of infected fish moved more slowly, were less cohesive, less aligned, and less temporally coordinated than non-infected pairs, and mixed pairs were primarily led by the non-infected fish. These social patterns also emerged in simulations of self-organised groups composed of individuals differing similarly in speed and turning tendency, suggesting infection-induced changes in mobility and manoeuvrability may drive collective outcomes. Together, our results demonstrate how infection with a complex life-cycle parasite affects the movement ability of individuals and how this in turn shapes social interaction patterns, providing important mechanistic insights into the effects of parasites on host movement dynamics.
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Comportamento Animal , Doenças dos Peixes/parasitologia , Interações Hospedeiro-Parasita , Smegmamorpha/parasitologia , Interação Social , AnimaisRESUMO
It is well recognized that environmental degradation caused by human activities can result in dramatic losses of species and diversity. However, comparatively little is known about the ability of biodiversity to re-emerge following ecosystem recovery. Here, we show that a European whitefish subspecies, the gangfisch Coregonus lavaretus macrophthalmus, rapidly increased its ecologically functional diversity following the restoration of Lake Constance after anthropogenic eutrophication. In fewer than ten generations, gangfisch evolved a greater range of gill raker numbers (GRNs) to utilize a broader ecological niche. A sparse genetic architecture underlies this variation in GRN. Several co-expressed gene modules and genes showing signals of positive selection were associated with GRN and body shape. These were enriched for biological pathways related to trophic niche expansion in fishes. Our findings demonstrate the potential of functional diversity to expand following habitat restoration, given a fortuitous combination of genetic architecture, genetic diversity and selection.
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Ecossistema , Recuperação e Remediação Ambiental , Salmonidae , Animais , Evolução Molecular , Feminino , Expressão Gênica , Genômica , Genótipo , Masculino , Fenótipo , Salmonidae/anatomia & histologia , Salmonidae/genéticaRESUMO
BACKGROUND: The evolution of reproductive traits, such as hybrid incompatibility (postzygotic isolation) and species recognition (prezygotic isolation), have shown their key role in speciation. Theoretical modeling has recently predicted that close linkage between genes controlling pre- and postzygotic reproductive isolation could accelerate the conditions for speciation. Postzygotic isolation could develop during the sympatric speciation process contributing to the divergence of populations. Using hybrid fitness as a measure of postzygotic reproductive isolation, we empirically studied population divergence in perch (Perca fluviatilis L.) from two genetically divergent populations within a lake. RESULTS: During spawning time of perch we artificially created parental offspring and F1 hybrids of the two populations and studied fertilization rate and hatching success under laboratory conditions. The combined fitness measure (product of fertilization rate and hatching success) of F1 hybrids was significantly reduced compared to offspring from within population crosses. CONCLUSION: Our results suggest intrinsic genetic incompatibility between the two populations and indicate that population divergence between two populations of perch inhabiting the same lake may indeed be promoted by postzygotic isolation.
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Predicting the evolution of phenotypic traits requires an understanding of natural selection on them. Despite its indispensability in the fight against parasites, selection on host immune defense has remained understudied. Theory predicts immune traits to be under stabilizing selection due to associated trade-offs with other fitness-related traits. Empirical studies, however, report mainly positive directional selection. This discrepancy could be caused by low phenotypic variation in the examined individuals and/or variation in host resource level that confounds trade-offs in empirical studies. In a field experiment where we maintained Lymnaea stagnalis snails individually in cages in a lake, we investigated phenotypic selection on two immune defense traits, phenoloxidase (PO)-like activity and antibacterial activity, in hemolymph. We used a diverse laboratory population and manipulated snail resource level by limiting their food supply. For six weeks, we followed immune activity, growth, and two fitness components, survival and fecundity of snails. We found that PO-like activity and growth were under stabilizing selection, while antibacterial activity was under positive directional selection. Selection on immune traits was mainly driven by variation in survival. The form of selection on immune defense apparently depends on the particular trait, possibly due to its importance for countering the present parasite community.
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Imunidade Inata , Lymnaea/genética , Lymnaea/imunologia , Seleção Genética , Animais , Antibacterianos/metabolismo , Fertilidade , Aptidão Genética , Hemolinfa/química , Longevidade , Lymnaea/enzimologia , Lymnaea/crescimento & desenvolvimento , Monofenol Mono-Oxigenase/metabolismoRESUMO
Subterranean biodiversity in Europe is spectacularly rich, with the Western Balkans being home to about 400 cave species, representing the highest number of species per area worldwide [1]. Nonetheless, cave fishes, which are the most commonly found vertebrates in underground habitats [2], have not been described from Europe so far [3]. Here, we report the first European record of a cave fish population, a loach of the genus Barbatula (Figure 1), found in the Danube-Aach system, an underground karst water system in Southern Germany [4]. The fish exhibit traits typically observed in organisms adapted to subterranean life including reduced eyes and pale body coloration [5]. The newly discovered population also represents globally the northernmost cave fish found so far. The geological history of the region implies that the Danube-Aach system was colonized post-glacially. A recent origin of the cave fish is supported by genetic analyses, because the subterranean population shares COI gene haplotypes with adjacent surface stone loach (Barbatula barbatula) populations (Figure 1D). Nonetheless, population genetic analyses based on microsatellites indicated that cave fish are genetically isolated from populations in surface habitats (Figure 1E) and exhibit reduced genetic variability. Hence, the newly discovered European cave loaches do not represent individuals displaced from surface populations, but they follow a unique evolutionary trajectory towards cave life.
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Adaptação Biológica , Evolução Biológica , Cipriniformes/fisiologia , Variação Genética , Características de História de Vida , Animais , Cavernas , Cipriniformes/genética , Alemanha , FilogeniaRESUMO
Stable isotope analysis of commercially and ecologically important fish can improve understanding of life-history and trophic ecology. However, accurate interpretation of stable isotope values requires knowledge of tissue-specific isotopic turnover that will help to describe differences in the isotopic composition of tissues and diet. We performed a diet-switch experiment using captive-reared parasite-free Eurasian perch (Perca fluviatilis) and wild caught specimens of the same species, infected with the pike tapeworm Triaenophorus nodulosus living in host liver tissue. We hypothesize that metabolic processes related to infection status play a major role in isotopic turnover and examined the influence of parasite infection on isotopic turn-over rate of carbon (δ13C), nitrogen (δ15N) and sulphur (δ34S) in liver, blood and muscle. The δ15N and δ13C turnovers were fastest in liver tissues, followed by blood and muscle. In infected fish, liver and blood δ15N and δ13C turnover rates were similar. However, in infected fish, liver and blood δ13C turnover was faster than that of δ15N. Moreover, in infected subjects, liver δ15N and δ13C turnover rates were three to five times faster than in livers of uninfected subjects (isotopic half-life of ca.3-4 days compared to 16 and 10 days, respectively). Blood δ34S turnover rate were about twice faster in non-infected individuals implying that parasite infection could retard the turnover rate of δ34S and sulphur containing amino acids. Slower turnover rate of essential amino acid could probably decrease individual immune function. These indicate potential hidden costs of chronic and persistent infections that may have accumulated adverse effects and might eventually impair life-history fitness. For the first time, we were able to shift the isotope values of parasites encapsulated in the liver by changing the dietary source of the host. We also report variability in isotopic turnover rates between tissues, elements and between infected and parasite-free individuals. These results contribute to our understanding of data obtained from field and commercial hatcheries; and strongly improve the applicability of the stable isotope method in understanding life-history and trophic ecology of fish populations.
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Isótopos de Carbono/análise , Cestoides , Infecções por Cestoides/metabolismo , Isótopos de Nitrogênio/análise , Percas/metabolismo , Percas/parasitologia , Isótopos de Enxofre/análise , Ração Animal , Animais , Comportamento Alimentar , Feminino , Meia-Vida , Lipídeos/sangue , Fígado/parasitologia , Masculino , Músculos/parasitologia , Fatores de TempoRESUMO
Genes that play key roles in host immunity such as the major histocompatibility complex (MHC) in vertebrates are expected to be major targets of selection. It is well known that environmental conditions can have an effect on host-parasite interactions and may thus influence the selection on MHC. We analyzed MHC class IIß variability over 35 years in a population of perch (Perca fluviatilis) from the Baltic Sea that was split into two populations separated from each other. One population was subjected to heating from cooling water of a nuclear power plant and was isolated from the surrounding environment in an artificial lake, while the other population was not subjected to any change in water temperature (control). The isolated population experienced a change of the allelic composition and a decrease in allelic richness of MHC genes compared to the control population. The two most common MHC alleles showed cyclic patterns indicating ongoing parasite-host coevolution in both populations, but the alleles that showed a cyclic behavior differed between the two populations. No such patterns were observed at alleles from nine microsatellite loci, and no genetic differentiation was found between populations. We found no indications for a genetic bottleneck in the isolated population during the 35 years. Additionally, differences in parasitism of the current perch populations suggest that a change of the parasite communities has occurred over the isolation period, although the evidence in form of in-depth knowledge of the change of the parasite community over time is lacking. Our results are consistent with the hypothesis of a selective sweep imposed by a change in the parasite community.
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Human-induced nutrient input can change the selection regime and lead to the loss of biodiversity. For example, eutrophication caused speciation reversal in polymorphic whitefish populations through a flattening of littoral-pelagic selection gradients. We investigated the current state of phenotypic and genetic diversity in whitefish (Coregonus macrophthalmus) in a newly restored lake whose nutrient load has returned to pre-eutrophication levels and found that whitefish spawning at different depths varied phenotypically and genetically: individuals spawning at shallower depth had fewer gill rakers, faster growth, and a morphology adapted to benthic feeding, and they showed higher degrees of diet specialization than deeper spawning individuals. Microsatellite analyses complemented the phenotype analyses by demonstrating reproductive isolation along different spawning depths. Our results indicate that whitefish still retain or currently regain phenotypic and genetic diversity, which was lost during eutrophication. Hence, the population documented here has a potential for future divergence because natural selection can target phenotypes specialized along re-established littoral-pelagic selection gradients. The biodiversity, however, will have better chances to return if managers acknowledge the evolutionary potential within the local whitefish and adapt fishing and stocking measures.
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Olfactory imprinting on environmental, population- and kin-specific cues is a specific form of life-long memory promoting homing of salmon to their natal rivers and the return of coral reef fish to natal sites. Despite its ecological significance, natural chemicals for olfactory imprinting have not been identified yet. Here, we show that MHC peptides function as chemical signals for olfactory imprinting in zebrafish. We found that MHC peptides consisting of nine amino acids elicit olfactory imprinting and subsequent kin recognition depending on the MHC genotype of the fish. In vivo calcium imaging shows that some olfactory bulb neurons are highly sensitive to MHC peptides with a detection threshold at 1â pM or lower, indicating that MHC peptides are potent olfactory stimuli. Responses to MHC peptides overlapped spatially with responses to kin odour but not food odour, consistent with the hypothesis that MHC peptides are natural signals for olfactory imprinting.
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Impressão Genômica/imunologia , Antígenos de Histocompatibilidade Classe II/imunologia , Peptídeos/imunologia , Olfato/genética , Olfato/imunologia , Peixe-Zebra/genética , Peixe-Zebra/imunologia , Alelos , Aminoácidos/farmacologia , Animais , Comportamento de Escolha/efeitos dos fármacos , Impressão Genômica/efeitos dos fármacos , Antígenos de Histocompatibilidade Classe I/genética , Antígenos de Histocompatibilidade Classe I/imunologia , Antígenos de Histocompatibilidade Classe II/genética , Larva/efeitos dos fármacos , Larva/imunologia , Ligantes , Neurônios/citologia , Neurônios/efeitos dos fármacos , Neurônios/metabolismo , Bulbo Olfatório/citologia , Peptídeos/farmacologia , Olfato/efeitos dos fármacos , Água/farmacologiaRESUMO
This article documents the addition of 238 microsatellite marker loci and 72 pairs of Single Nucleotide Polymorphism (SNP) sequencing primers to the Molecular Ecology Resources Database. Loci were developed for the following species: Adelges tsugae, Artemisia tridentata, Astroides calycularis, Azorella selago, Botryllus schlosseri, Botrylloides violaceus, Cardiocrinum cordatum var. glehnii, Campylopterus curvipennis, Colocasia esculenta, Cynomys ludovicianus, Cynomys leucurus, Cynomys gunnisoni, Epinephelus coioides, Eunicella singularis, Gammarus pulex, Homoeosoma nebulella, Hyla squirella, Lateolabrax japonicus, Mastomys erythroleucus, Pararge aegeria, Pardosa sierra, Phoenicopterus ruber ruber and Silene latifolia. These loci were cross-tested on the following species: Adelges abietis, Adelges cooleyi, Adelges piceae, Pineus pini, Pineus strobi, Tubastrea micrantha, three other Tubastrea species, Botrylloides fuscus, Botrylloides simodensis, Campylopterus hemileucurus, Campylopterus rufus, Campylopterus largipennis, Campylopterus villaviscensio, Phaethornis longuemareus, Florisuga mellivora, Lampornis amethystinus, Amazilia cyanocephala, Archilochus colubris, Epinephelus lanceolatus, Epinephelus fuscoguttatus, Symbiodinium temperate-A clade, Gammarus fossarum, Gammarus roeselii, Dikerogammarus villosus and Limnomysis benedeni. This article also documents the addition of 72 sequencing primer pairs and 52 allele specific primers for Neophocaena phocaenoides.
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This study provides the first investigation of the diversity, structure, and molecular evolution of MHII beta genes in a non-model percid species -- the Eurasian perch (Perca fluviatilis L.). PCR primers developed here were highly specific, and documented a high diversity of the MHII beta1 domain in perch. Our results suggest a minimum of eight MHII beta loci in this species -- a finding congruent with several studies suggesting that many Euteleostei posses multiple MHII beta loci. As for other vertebrates, both positive selection and gene-conversion contribute to the reported high allelic diversity. Similarly, the MHII beta1 domain in perch exhibits a characteristic MHC fold known from other vertebrates. In addition, our results suggest some teleost specific differences of the MHII beta1 domain, including: differences in chemical properties of specific amino acids in the beta1 domain, the absence of the tetrapod specific glycolisation signal, and differences in the positions of some of the positively selected codons in the MHII beta1 domain, which are presumably involved in antigen binding. Future studies should investigate the teleost MHII beta genes in more details in order to confirm the suggested differences, and to determine the extent to which these differences prevail in different teleost lineages.