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Reproductive isolation, evolutionary distinctiveness and setting conservation priorities: the case of European lake whitefish and the endangered North Sea houting (Coregonus spp.).

ABSTRACT: BACKGROUND:Adaptive radiation within fishes of the Coregonus lavaretus complex has created numerous morphs, posing significant challenges for taxonomy and conservation priorities. The highly endangered North Sea houting (C. oxyrhynchus; abbreviated NSH) has been considered a separate species from European lake whitefish (C. lavaretus; abbreviated ELW) due to morphological divergence and adaptation to oceanic salinities. However, its evolutionary and taxonomic status is controversial. We analysed microsatellite DNA polymorphism in nine populations from the Jutland Peninsula and the Baltic Sea, representing NSH (three populations, two of which are reintroduced) and ELW (six populations). The objectives were to: 1) analyse postglacial recolonization of whitefish in the region; 2) assess the evolutionary distinctiveness of NSH, and 3) apply several approaches for defining conservation units towards setting conservation priorities for NSH. RESULTS:Bayesian cluster analyses of genetic differentiation identified four major groups, corresponding to NSH and three groups of ELW (Western Jutland, Central Jutland, Baltic Sea). Estimates of historical migration rates indicated recolonization in a north-eastern direction, suggesting that all except the Baltic Sea population predominantly represent postglacial recolonization via the ancient Elbe River. Contemporary gene flow has not occurred between NSH and ELW, with a divergence time within the last 4,000 years suggested from coalescence methods. NSH showed interbreeding with ELW when brought into contact by stocking. Thus, reproductive isolation of NSH was not absolute, although possible interbreeding beyond the F1 level could not be resolved. CONCLUSION:Fishes of the C. lavaretus complex in the Jutland Peninsula originate from the same recolonization event. NSH has evolved recently and its species status may be questioned due to incomplete reproductive isolation from ELW, but it was shown to merit consideration as an independent conservation unit. Yet, application of several approaches for defining conservation units generated mixed outcomes regarding its conservation priority. Within the total species complex, it remains one among many recently evolved unique forms. Its uniqueness and high conservation priority is more evident at a local geographical scale, where conservation efforts will also benefit populations of a number of other endangered species.

SUBMITTER: Hansen MM

PROVIDER: S-EPMC2396634 | biostudies-literature | 2008 May

REPOSITORIES: biostudies-literature

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Reproductive isolation, evolutionary distinctiveness and setting conservation priorities: the case of European lake whitefish and the endangered North Sea houting (Coregonus spp.).

Hansen Michael M MM Fraser Dylan J DJ Als Thomas D TD Mensberg Karen-Lise D KL

BMC evolutionary biology 20080509

<h4>Background</h4>Adaptive radiation within fishes of the Coregonus lavaretus complex has created numerous morphs, posing significant challenges for taxonomy and conservation priorities. The highly endangered North Sea houting (C. oxyrhynchus; abbreviated NSH) has been considered a separate species from European lake whitefish (C. lavaretus; abbreviated ELW) due to morphological divergence and adaptation to oceanic salinities. However, its evolutionary and taxonomic status is controversial. We ...[more]

PMID: 18471278

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Project description: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 twentieth 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.

Project description:We used microarrays and a previously established linkage map to localize the genetic determinants of brain gene expression for a backcross family of lake whitefish species pairs (Coregonus sp.). Our goals were to elucidate the genomic distribution and sex-specificity of brain expression QTL (eQTL) and to determine the extent to which genes controlling transcriptional variation may underlie adaptive divergence in the recently evolved dwarf (limnetic) and normal (benthic) whitefish. We observed a sex-bias in transcriptional genetic architecture, with more eQTL observed in males, as well as divergence in genome location of eQTL between sexes. Hotspots of nonrandom aggregations of up to 32 eQTL in one location were observed. We identified candidate genes for species pair divergence involved with energetic metabolism, protein synthesis, and neural development based on co-localization of eQTL for these genes with eight previously identified adaptive phenotypic QTL and four previously identified outlier loci from a genome scan in natural populations. 88% of eQTL-phenotypic QTL co-localization involved growth rate and condition factor QTL, two traits central to adaptive divergence between whitefish species pairs. Hotspots co-localized with phenotypic QTL in several cases, revealing possible locations where master regulatory genes, such as a zinc finger protein in one case, control gene expression directly related to adaptive phenotypic divergence. We observed little evidence of co-localization of brain eQTL with behavioral QTL, which provides insight on the genes identified by behavioral QTL studies. These results extend to the transcriptome level previous work illustrating that selection has shaped recent parallel divergence between dwarf and normal lake whitefish species pairs and that metabolic, more than morphological differences appear to play a key role in this divergence. Keywords: eQTL mapping, gene expression, linkage mapping, adaptive radiation, Coregonus, microarrays The objective of this study was to elucidate the genomic distribution and sex-specificity of brain eQTL in dwarf and normal lake whitefish. Dissected brain tissue (250-350 mg) was sampled for 55 individuals from a hybrid x dwarf backcross mapping family. We used a loop design (YANG and SPEED 2002; CHURCHILL 2002) to maximize the number of sampled meioses. Each of 55 samples was technically replicated on two distinct slides, while performing dye swapping (Cy3 and Alexa) to estimate the dye intensity variation bias. After correcting for local background, raw intensity values were both log2 transformed and normalized using the regional LOWESS method implemented in the R/MANOVA software (KERR et al. 2000). We used a previously generated linkage map based on the same backcross individuals for which gene expression was measured. eQTL mapping was performed with QTL Cartographer.

Project description:Genetic analyses of speciation have focused nearly exclusively on retrospective analyses of reproductive isolation between highly divergent species. Yet, a full understanding of the speciation process must encompass analysis of the consequences of genomic divergence in young lineages still capable of exchanging genes under natural conditions. The accumulation of conditionally neutral genetic variation may lead to the evolution of divergent gene networks. In a hybrid background, such mutations may no longer compensate one another, resulting in the appearance of selectively disadvantageous traits, including disruption of gene expression regulation. Here, we documented genome-wide patterns of gene expression divergence between young lineages of normal and dwarf lake whitefish and their backcross hybrids for which strong, yet incomplete post-zygotic isolation barriers exist. A significant proportion (33%) of backcross hybrids showed developmental abnormalities not seen in parental forms and eventually leading to death. While the transcriptome of parental forms was nearly identical during embryonic development, suggesting a role for stabilizing selection, all hybrids displayed strongly divergent patterns of gene expression. By comparing healthy, surviving hybrids against moribund ones, we observed that over 2000 genes were misregulated in these abnormal embryos. In particular, misregulation was significantly biased towards essential developmental genes which were strongly underexpressed. Furthermore, genes previously documented to be highly transgressive (exaggerated inter-individual variance) were almost invariably underexpressed in hybrids. Our results thus clearly showed a transcriptome-wide signature of hybrid breakdown in young, incipient species and demonstrated a persuasive link between misexpression of essential developmental genes and post zygotic isolation. Samples of dwarf, normal, backcross-healthy and backcross-moribund were hybridized in a loop design, involving eight biological replicates for the backcross-healthy and backcross-moribund comparison and six for the others. Dye swap was performed between each replicate. As a result, we obtained a final set of 32 microarray slides.

Dataset Information

Reproductive isolation, evolutionary distinctiveness and setting conservation priorities: the case of European lake whitefish and the endangered North Sea houting (Coregonus spp.).

Publications

Reproductive isolation, evolutionary distinctiveness and setting conservation priorities: the case of European lake whitefish and the endangered North Sea houting (Coregonus spp.).

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