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Underwater video of lake whitefish Coregonus clupeaformis spawning in lake Michigan
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Data from: Ecological speciation in European whitefish is driven by a large‐gaped predator
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Data from: Genetic correlations and little genetic variance for reaction norms may limit potential for adaptation to pollution by ionic and nanoparticulate silver in a whitefish (Salmonidae)
For natural populations to adapt to anthropogenic threats, heritable variation must persist in tolerance traits. Silver nanoparticles, the most widely used engineered nanoparticles, are expected to increase in concentrations in freshwaters. Little is known about how these particles affect wild populations, and whether genetic variation persists in tolerance to permit rapid evolutionary responses. We sampled wild adult whitefish and crossed them in vitro full factorially. In total, 2896 singly raised embryos of 48 families were exposed to two concentrations (0.5 μg/L; 100 μg/L) of differently sized silver nanoparticles or ions (silver nitrate). These doses were not lethal; yet higher concentrations prompted embryos to hatch earlier and at a smaller size. The induced hatching did not vary with nanoparticle size and was stronger in the silver nitrate group. Additive genetic variation for hatching time was significant across all treatments, with no apparent environmental dependencies. No genetic variation was found for hatching plasticity. We found some treatment-dependent heritable variation for larval length and yolk volume, and one instance of additive genetic variation for the reaction norm on length at hatching. Our assessment suggests that the effects of silver exposure on additive genetic variation vary according to trait and silver source. While the long-term fitness consequences of low-level silver exposure on whitefish embryos must be further investigated to determine whether it is, in fact, detrimental, our results suggest that the evolutionary potential for adaptation to these types of pollutants may be low.
Data from: Adaptation and acclimation of aerobic exercise physiology in Lake Whitefish ecotypes (Coregonus clupeaformis)
The physiological mechanisms underlying local adaptation in natural populations of animals, and whether the same mechanisms contribute to adaptation and acclimation, are largely unknown. Therefore, we tested for evolutionary divergence in aerobic exercise physiology in laboratory bred, size-matched crosses of ancestral, benthic, normal Lake Whitefish (Coregonus clupeaformis) and derived, limnetic, more actively-swimming 'dwarf' ecotypes. We acclimated fish to constant swimming (emulating limnetic foraging) and control conditions (emulating normal activity levels) to simultaneously study phenotypic plasticity. We found extensive divergence between ecotypes: dwarf fish generally had constitutively higher values of traits related to oxygen transport (ventricle size) and use by skeletal muscle (percent oxidative muscle, mitochondrial content), and also evolved differential plasticity of mitochondrial function (Complex I activity and flux through Complexes I-IV and IV). The effects of swim-training were less pronounced than differences among ecotypes and the traits which had a significant training effect (ventricle protein content, ventricle MDH activity and muscle Complex V activity) did not differ among ecotypes. Only one trait, ventricle mass, varied in a similar manner with acclimation and adaptation and followed a pattern consistent with genetic accommodation. Overall, the physiological and biochemical mechanisms underlying acclimation and adaptation to swimming activity in Lake Whitefish generally differ.
Data from: MHC class I expression dependent on bacterial infection and parental factors in whitefish embryos (Salmonidae)
Ecological conditions can influence not only the expression of a phenotype, but also the heritability of a trait. As such, heritable variation for a trait needs to be studied across environments. We have investigated how pathogen challenge affects the expression of MHC genes in embryos of the lake whitefish Coregonus palaea. In order to experimentally separate paternal (i.e. genetic) from maternal and environmental effects, and determine whether and how stress affects the heritable variation for MHC expression, embryos were produced in full-factorial in vitro fertilizations, reared singly, and exposed at 208 degree days (late-eyed stage) to either one of two strains of Pseudomonas fluorescens that differ in their virulence characteristics (one increased mortality, while both delayed hatching time). Gene expression was assessed 48 h postinoculation, and virulence effects of the bacterial infection were monitored until hatching. We found no evidence of MHC class II expression at this stage of development. MHC class I expression was markedly down-regulated in reaction to both pseudomonads. While MHC expression could not be linked to embryo survival, the less the gene was expressed, the earlier the embryos hatched within each treatment group, possibly due to trade-offs between immune function and developmental rate or further factors that affect both hatching timing and MHC expression. We found significant additive genetic variance for MHC class I expression in some treatments. That is, changes in pathogen pressures could induce rapid evolution in MHC class I expression. However, we found no additive genetic variance in reaction norms in our study population.
Data from: Phenotypic and genetic divergence within a single whitefish form – detecting the potential for future divergence
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 re-gain 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.
Data from: Gene coexpression networks reveal key drivers of phenotypic divergence in lake whitefish
BACKGROUND: A functional understanding of processes involved in adaptive divergence is one of the awaiting opportunities afforded by high throughput transcriptomic technologies. Functional analysis of co-expressed genes has succeeded in the biomedical field in identifying key drivers of disease pathways. However, in ecology and evolutionary biology, functional interpretation of transcriptomic data is still limited. RESULTS: Here we used Weighted Gene Co-Expression Network Analysis (WGCNA) to identify modules of co-expressed genes in muscle and brain tissue of a lake whitefish backcross progeny. Modules were connected to gradients of known adaptive traits involved in the ecological speciation process between benthic and limnetic ecotypes. Key drivers, i.e. hub genes of functional modules related to reproduction, growth, and behavior were identified, and module preservation was assessed in natural populations. Using this approach, we identified modules of co-expressed genes involved in phenotypic divergence and their key drivers, and further identified a module part specifically rewired in the backcross progeny. CONCLUSIONS: Functional analysis of transcriptomic data can significantly contribute to the understanding of the mechanisms underlying ecological speciation. Our findings point to BMP and Calcium signaling as common pathways involved in coordinated evolution of trophic behavior, trophic morphology (gill rakers), and reproduction. Results also point to pathways implicating hemoglobins and constitutive stress response (HSP70) governing growth in lake whitefish.
Data from: The genetic architecture of reproductive isolation during speciation-with-gene-flow in lake whitefish species pairs assessed by RAD sequencing
During speciation-with-gene-flow, effective migration varies across the genome as a function of several factors, including proximity of selected loci, recombination rate, strength of selection, and number of selected loci. Genome scans may provide better empirical understanding of the genome-wide patterns of genetic differentiation, especially if the variance due to the previously mentioned factors is partitioned. In North American lake whitefish (Coregonus clupeaformis), glacial lineages that diverged in allopatry about 60,000 years ago and came into contact 12,000 years ago have independently evolved in several lakes into two sympatric species pairs (a normal benthic and a dwarf limnetic). Variable degrees of reproductive isolation between species pairs across lakes offer a continuum of genetic and phenotypic divergence associated with adaptation to distinct ecological niches. To disentangle the complex array of genetically based barriers that locally reduce the effective migration rate between whitefish species pairs, we compared genome-wide patterns of divergence across five lakes distributed along this divergence continuum. Using restriction site associated DNA (RAD) sequencing, we combined genetic mapping and population genetics approaches to identify genomic regions resistant to introgression and derive empirical measures of the barrier strength as a function of recombination distance. We found that the size of the genomic islands of differentiation was influenced by the joint effects of linkage disequilibrium maintained by selection on many loci, the strength of ecological niche divergence, as well as demographic characteristics unique to each lake. Partial parallelism in divergent genomic regions likely reflected the combined effects of polygenic adaptation from standing variation and independent changes in the genetic architecture of postzygotic isolation. This study illustrates how integrating genetic mapping and population genomics of multiple sympatric species pairs provide a window on the speciation-with-gene-flow mechanism.
Data from: Contemporary factors influencing genetic diversity in the Alaska humpback whitefish Coregonus clupeaformis complex
Thirteen microsatellite loci were used to address three hypotheses regarding genetic diversity in the humpback whitefish Coregonus clupeaformis complex in Alaska. The test results provided further insight into the factors influencing C. clupeaformis complex population structure and level of genetic variation. First, themicrosatellite data did not provide evidence of two spatially distinct Beringian and Eurasian refugial groups as revealed in previous phylogeographic analyses ofmitochondrialDNAvari- ation. Rather, the population structure inferred from the microsatellite variation appears to reveal the influence of factors on amore recent time scale, including gene flowamong the refugial groups and iso- lation of some anadromous and freshwater resident populations. Second, anadromous C. clupeaformis complex collections exhibited higher intra-population genetic diversity than freshwater resident col- lections. This outcome is consistent with previous meta analyses suggesting that freshwater resident populations probably have smaller historical effective population sizes and less conspecific gene flow because the habitat tends to be smaller and supports fewer and smaller populations. Finally, the analy- sis of contemporary immigration rates was consistent with, but did not provide statistical support for, the hypothesis that gene flow among anadromous C. clupeaformis complex populations along coastal Alaska is influenced by the Alaska Coastal Current. Further studies are needed to evaluate gene flow among coastal Alaska C. clupeaformis complex populations. Published
Data from: The transcriptomics of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis spp., Salmonidae) divergence as revealed by next-generation sequencing
Gene expression divergence is one of the mechanisms thought to be involved in the emergence of incipient species. Next-generation sequencing has become an extremely valuable tool for the study of this process by allowing whole transcriptome sequencing, or RNA-Seq. We have conducted a 454 GS-FLX pyrosequencing experiment in order to refine our understanding of adaptive divergence between dwarf and normal lake whitefish species (Coregonus clupeaformis spp.). The objectives were to: (1) investigate transcriptomic divergence as measured by liver RNA-Seq; (2) test the correlation between divergence in expression and sequence polymorphism and (3) investigate the extent of allelic imbalance. We also compared the results of RNA-seq with those of a previous microarray study performed on the same fish. Following de novo assembly, results showed that normal whitefish over-expressed more contigs associated with protein synthesis while dwarf fish over-expressed more contigs related to energy metabolism, immunity and DNA replication and repair. Moreover, 63 SNPs showed significant allelic imbalance, and this phenomenon prevailed in the recently diverged dwarf whitefish. Results also showed an absence of correlation between gene expression divergence as measured by RNA-Seq and either polymorphism rate or sequence divergence between normal and dwarf whitefish. This study reiterates an important role for gene expression divergence, and provides evidence for allele-specific expression divergence as well as evolutionary decoupling of regulatory and coding sequences in the adaptive divergence of normal and dwarf whitefish. It also demonstrates how next-generation sequencing can lead to a more comprehensive understanding of transcriptomic divergence in a young species pair.
Data from: Oxidative phosphorylation gene transcription in whitefish species pairs reveals patterns of parallel and non-parallel physiological divergence
Across multiple lakes in North America, lake whitefish (Coregonus clupeaformis) have independently evolved "dwarf" and "normal" sympatric species pairs that exhibit pronounced phenotypic and genetic divergence. In particular, traits associated with metabolism have been shown to be highly differentiated between whitefish species. Here, we examine the transcription of genes associated with all five mitochondrial and nuclear genome-encoded oxidative phosphorylation (OXPHOS) complexes, the primary physiological mechanism responsible for the production of ATP, in whitefish species pairs from Cliff Lake and Webster Lake in Maine, USA. We observed OXPHOS gene transcription divergence between dwarf and normal whitefish in each of the two lakes, with the former exhibiting transcription upregulation for genes associated with each of the OXPHOS complexes. We also observed a significant influence of lake on transcription levels for some of the genes, indicating that inter-lake ecological or genetic differences are contributing to variation in OXPHOS gene transcription levels. Together, our results support the hypothesis that metabolic divergence is a critical adaptation involved in whitefish speciation, and implicate OXPHOS gene upregulation as a factor involved in meeting the enhanced energetic demands of dwarf whitefish. Further examination of the links between this critical physiological pathway and ecological and genetic variation will provide insight into the fine-scale evolutionary dynamics at work in nature.
Data from: Testing the devil's impact on southern Baltic and North Sea basin whitefish (Coregonus spp.) diversity
Background: The diversity and phylogeny of whitefish of the genus Coregonus is complex, and includes many endemic species of high conservation concern. However, because of commercial importance of whitefish fisheries, stockings and translocations have occurred repeatedly, which challenges the identification of local populations as conservation units. This study analyses the phylogenetic relationships of 15 contemporary and two historical populations of lake-resident and anadromous whitefish (Coregonus spp.) from the southern Baltic and North Sea basins. We elucidated the complex history of Lake Schaal (northern Germany) whitefish, for which a local tale suggests that the devil threw whitefish from the Central European Lake Constance into this lake. Studies from the early 20th century indeed suggested numerous stocking events for Lake Schaal from Lake Constance, from Estonian/Russian Lake Peipsi and from the anadromous whitefish of the Baltic Sea. Results: Analyses of 13 microsatellite markers showed that Lake Constance whitefish are unrelated to any northern Germany whitefish population, including the contemporary whitefish population from Lake Schaal. Comparison with four historical specimens further showed that the native Lake Schaal whitefish (C. holsatus) vanished from the lake, but has survived as a non-native population in the north German Lake Drewitz. The whitefish currently occurring in Lake Schaal and three adjacent lakes are identified as C. maraenoides, introduced from Lake Peipsi. The contemporary anadromous whitefish populations from the Baltic (German and Finnish coast) and the German River Treene (North Sea basin, stocked from Danish River Vida) grouped together, but showed significant genetic differentiation. The 14 historical specimens of C. oxyrinchus from Rivers Rhine and Schelde were assigned to several contemporary whitefish populations, but among them only one specimen was assigned to the contemporary River Treene population. Therefore, we do not support the view that the whitefish from River Vida/Treene are identical with the historical C. oxyrinchus. Conclusions: Our study demonstrates that lake and anadromous whitefish in the Baltic and North Sea basins reflect a complex phylogeography, which is further blurred by the effects of repeated stocking and translocations. To identify conservation units, the genetic identity of each population has to be scrutinized.
Data from: Coexistence and origin of trophic ecotypes of pygmy whitefish, Prosopium coulterii, in southwestern Alaskan lake
Ecologically, morphologically, and genetically distinct populations within single taxa often co-exist in postglacial lakes and have provided important model systems with which to investigate ecological and evolutionary processes such as niche partitioning and ecological speciation. Within the Salmonidae, these species complexes have been well studied, particularly within the Coregonus clupeaformis-C. laveratus (lake and European whitefish, respectively) group, but the phenomenon has been less well documented in the other whitefish genera, Prosopium and Stenodus. Here, we examined the morphology, feeding biology, and genetic structure of three putative forms of the pygmy whitefish, Prosopium coulterii, that were first reported from Chignik Lake, southwestern Alaska, over 40 years ago. Field collections and morphological analyses resolved a shallow water (< 5 m depth) low gill raker count form (< 15 first arch gill rakers), a deepwater (> 30 m), low gill raker form, and a deepwater, high gill raker count (> 15 gill rakers) form. The two low gill raker count forms fed almost exclusively on benthic invertebrates (mostly chironomids), while the deepwater, high gill raker count form fed almost exclusively on zooplankton, differences in diet that were also reflected in differences both in δ13C and δ15N stable isotopes. All three forms were characterized by the same major mitochondrial DNA clade that has been associated with persistence in, and postglacial dispersal from, a Beringian glacial refugium. Analysis of variation at nine microsatellite DNA loci indicated low, but significant differentiation amongst forms, especially between the two low gill raker count forms and the high gill raker count form. The extent of differentiation along phenotypic (considerable) and genetic (subtle) axes amongst the Chignik Lake forms is similar to that found amongst distinct taxa of Prosopium found in pre-glacial Bear Lake (Utah-Idaho, USA) which is probably at least ten times older than Chignik Lake. Our analyses illustrate the potential for the postglacial differentiation in traits subject to divergent natural selection across variable environments.
Data from: Convergence in organ size but not energy metabolism enzyme activities among wild Lake Whitefish (Coregonus clupeaformis) species pairs
The repeated evolution of similar phenotypes by similar mechanisms can be indicative of local adaptation, constraints or biases in the evolutionary process. Little is known about the incidence of physiological convergence in natural populations, so here we test whether energy metabolism in 'dwarf' and 'normal' Lake Whitefish evolves by similar mechanisms. Prior genomic and transcriptomic studies have found that divergence in energy metabolism is key to local adaptation in whitefish species pairs, but that distinct genetic and transcriptomic changes often underlie phenotypic evolution among lakes. Here, we predicted that traits at higher levels of biological organization, including the activities of energy metabolism enzymes (the product of enzyme concentration and turnover rate) and the relative proportions of metabolically active tissues (heart, liver, skeletal muscle), would show greater convergence than genetic and transcriptomic variation. We compared four whitefish species pairs and found convergence in organ size whereby all dwarf whitefish populations have a higher proportion of red skeletal muscle, three have relatively larger livers and two have relatively larger ventricles than normal fish. On the other hand, hepatic and muscle enzyme activities showed little convergence and were largely dependent on lake of origin. Only the most genetically divergent species pair (Cliff Lake) displayed white muscle enzyme activities matching results from laboratory-reared normal and dwarf whitefish. Overall, these data show convergence in the evolution of organ size, but not in the activities of candidate enzymes of energy metabolism, which may have evolved mainly as a consequence of demographic or ecological differences among lakes.
Data from: Maternal and paternal contributions to pathogen resistance dependent on development stage in a whitefish (Salmonidae)
1. It is often assumed that maternal and paternal contributions to offspring phenotype change over the lifetime of an individual. However, studies on parental effects typically suffer from the problems that heritabilities and maternal environmental effects are difficult to separate, and that both may depend on environmental factors and developmental stage 2. In order to experimentally disentangle maternal from paternal contributions and the likely effects of developmental stage from ecological effects, we sampled a natural population of the whitefish Coregonus palaea, used gametes for full-factorial in vitro fertilizations, raised over 10,000 of the resulting offspring singly at controlled conditions, and exposed them at different points during embryonic development to one of two strains of Pseudomonas fluorescens that differed in their virulence characteristics (only one caused mortality, while both delayed hatching and reduced growth) 3. Vulnerability to infection increased markedly over embryo development. This change coincided with a distinct shift in the importance of maternal to additive genetic effects on survival. Timing of exposure also affected the variance components for hatching time and larval length, but in a less consistent direction than the variance components for mortality. No significant genetic variation was found for any reaction norms across time points of exposure, indicating a uniformity among genotypes in how susceptibility changed over development. Phenotypes were also typically correlated across time points, which could constrain the evolution of the reaction norms 4. Our experiment demonstrates that the relative maternal and paternal contributions to susceptibility to an infection, and hence the evolutionary potential to respond to pathogen-induced selection, depends not only on the kind of pathogenic stress but also on the timing of the challenge.
Data from: Genetic population structure of the round whitefish (Prosopium cylindraceum) in North America: multiple markers reveal glacial refugia and regional subdivision.
Round whitefish (Prosopium cylindraceum) have a broad, disjunct range across northern North America and Eurasia, and little is known about their genetic population structure. We performed genetic analyses of round whitefish from 17 sites across its range using nine microsatellites, two mitochondrial DNA (mtDNA) loci, and 4918 to 8835 single-nucleotide polymorphism (SNP) loci. Our analyses identified deep phylogenetic division between eastern and western portions of the range, likely indicative of origins from at least two separate Pleistocene glacial refugia. Regionally, microsatellites and SNPs identified congruent patterns in subdivision, and population structure was consistent with expectations based on hydrologic connectivity. Within the Laurentian Great Lakes, Lake Huron and Lake Ontario were identified as key areas of interest. Lake Huron appears to be a contemporary source population for several other Great Lakes, and Lake Ontario contains a genetically discrete group of round whitefish. In all cases, multiple genetic markers yielded similar patterns, but SNPs offered substantially enhanced resolution. We conclude that round whitefish have population subdivision on several scales important for understanding their evolutionary history and conservation planning.
Supplementary material 1 from: Selz OM, Seehausen O (2023) A taxonomic revision of ten whitefish species from the lakes Lucerne, Sarnen, Sempach and Zug, Switzerland, with descriptions of seven new species (Teleostei, Coregonidae). ZooKeys 1144: 95-169. https://doi.org/10.3897/zookeys.1144.67747
Historical and contemporary notes on C. sarnensis, C. litoralis, C. nobilis, Lake Zug whitefish and on different topics in the discussion of the main manuscript.
Data from: The transcriptomics of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis spp., Salmonidae) divergence as revealed by next-generation sequencing
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Data from: Adaptation and acclimation of aerobic exercise physiology in Lake Whitefish ecotypes (Coregonus clupeaformis)
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Data from: Genetic population structure of the round whitefish (Prosopium cylindraceum) in North America: multiple markers reveal glacial refugia and regional subdivision.
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