Kim Præbel

Ecological speciation in postglacial European whitefish: rapid adaptive radiations into the littoral, pelagic, and profundal lake habitats

Understanding how a monophyletic lineage of a species diverges into several adaptive forms has received increased attention in recent years, but the underlying mechanisms in this process are still under debate. Postglacial fishes are excellent model organisms for exploring this process, especially the initial stages of ecological speciation, as postglacial lakes represent replicated discrete environments with variation in available niches. Here, we combine data of niche utilization, trophic morphology, and 17 microsatellite loci to investigate the diversification process of three sympatric European whitefish morphs from three northern Fennoscandian lakes. The morphological divergence in the gill raker number among the whitefish morphs was related to the utilization of different trophic niches and was associated with reproductive isolation within and across lakes. The intralacustrine comparison of whitefish morphs showed that these systems represent two levels of adaptive divergence: (1) a consistent littoral–pelagic resource axis; and (2) a more variable littoral–profundal resource axis. The results also indicate that the profundal whitefish morph has diverged repeatedly from the ancestral littoral whitefish morph in sympatry in two different watercourses. In contrast, all the analyses performed revealed clustering of the pelagic whitefish morphs across lakes suggesting parallel postglacial immigration with the littoral whitefish morph into each lake. Finally, the analyses strongly suggested that the trophic adaptive trait, number of gill rakers, was under diversifying selection in the different whitefish morphs. Together, the results support a complex evolutionary scenario where ecological speciation acts, but where both allopatric (colonization history) and sympatric (within watercourse divergence) processes are involved.

Parallel and non-parallel morphological divergence among foraging specialists in European whitefish (Coregonus lavaretus).

Parallel phenotypic evolution occurs when independent populations evolve similar traits in response to similar selective regimes. However, populations inhabiting similar environments also frequently show some phenotypic differences that result from non-parallel evolution. In this study, we quantified the relative importance of parallel evolution to similar foraging regimes and non-parallel lake-specific effects on morphological variation in European whitefish (Coregonus lavaretus). We found evidence for both lake-specific morphological characteristics and parallel morphological divergence between whitefish specializing in feeding on profundal and littoral resources in three separate lakes. Foraging specialists expressed similar phenotypes in different lakes in both overall body shape and selected measured morphological traits. The morphology of the two whitefish specialists resembled that predicted from other fish species, supporting the conclusion of an adaptive significance of the observed morphological characteristics. Our results indicate that divergent natural selection resulting from foraging specialization is driving and/or maintaining the observed parallel morphological divergence. Whitefish in this study may represent an early stage of divergence towards the evolution of specialized morphs.

Speciation Reversal in European Whitefish (Coregonus lavaretus (L.)) Caused by Competitor Invasion

Invasion of exotic species has caused the loss of biodiversity and imparts evolutionary and ecological changes in the introduced systems. In northern Fennoscandia, European whitefish (Coregonus lavaretus (L.)) is a highly polymorphic species displaying adaptive radiations into partially reproductively isolated and thus genetically differentiated sympatric morphs utilizing the planktivorous and benthivorous food niche in many lakes. In 1993, Lake Skrukkebukta was invaded by vendace (Coregonus albula (L.)) which is a zooplanktivorous specialist. The vendace displaced the densely rakered whitefish from its preferred pelagic niche to the benthic habitat harbouring the large sparsely rakered whitefish. In this study, we investigate the potential influence of the vendace invasion on the breakdown of reproductive isolation between the two whitefish morphs. We inferred the genotypic and phenotypic differentiation between the two morphs collected at the arrival (1993) and 15 years after (2008) the vendace invasion using 16 microsatellite loci and gill raker numbers, the most distinctive adaptive phenotypic trait between them. The comparison of gill raker number distributions revealed two modes growing closer over 15 years following the invasion. Bayesian analyses of genotypes revealed that the two genetically distinct whitefish morphs that existed in 1993 had collapsed into a single population in 2008. The decline in association between the gill raker numbers and admixture values over 15 years corroborates the findings from the Bayesian analysis. Our study thus suggests an apparent decrease of reproductive isolation in a morph-pair of European whitefish within 15 years (≃ 3 generations) following the invasion of a superior trophic competitor (vendace) in a subarctic lake, reflecting a situation of “speciation in reverse”.

Parallelism in the oxygen transport system of the lake whitefish: the role of physiological divergence in ecological speciation

In North America, populations of lake whitefish (Coregonus clupeaformis) have evolved sympatric ‘dwarf’ and ‘normal’ ecotypes that are associated with distinct trophic niches within lakes. Trophic specialization should place diverging physiological demands on individuals, and thus, genes and phenotypes associated with energy production represent ideal candidates for studies of adaptation. Here, we test for the parallel divergence of traits involved in oxygen transport in dwarf and normal lake whitefish from Québec, Canada and Maine, USA. We observed significant differences in red blood cell morphology between the ecotypes. Specifically, dwarfs exhibited larger nuclei and a higher nucleus area/total cell area than normal whitefish in all of the lakes examined. In addition, isoelectric focusing gels revealed variation in the haemoglobin protein components found in whitefish. Dwarf and normal whitefish exhibited a similar number of protein components, but the composition of these components differed, with dwarf whitefish bearing a greater proportion of cathodic components compared to the normals. Furthermore, dwarf whitefish showed significant haemoglobin gene upregulation in the brain compared with the levels shown in normals. Together, our results indicate that metabolic traits involved in oxygen transport differ between the whitefish ecotypes and the strong parallel patterns of divergence observed across lakes implicates ecologically driven selection pressures. We discuss the function of these traits in relation to the differing trophic niches occupied by the whitefish and the potential contributions of trait plasticity and genetic divergence to energetic adaptation.

Discrete foraging niches promote ecological, phenotypic, and genetic divergence in sympatric whitefish (Coregonus lavaretus)

Natural populations often vary in their degree of ecological, morphological and genetic divergence. This variation can be arranged along an ecological speciation continuum of increasingly discrete variation, with high inter-individual variation at one end and well defined species in the other. In postglacial fishes, evolutionary divergence has commonly resulted in the co-occurrence of a pelagic and a benthic specialist. We studied three replicate lakes supporting sympatric pelagic and benthic European whitefish (Coregonus lavaretus (L.)) morphs in search for early signs of possible further divergence into more specialized niches. Using stomach content data (recent diet) and stable isotope analyses (time-integrated measure of trophic niche use), we observed a split in the trophic niche within the benthic whitefish morph, with individuals specializing on either littoral or profundal resources. This divergence in resource use was accompanied by small but significant differences in an adaptive morphological trait (gill raker number) and significant genetic differences between fish exploiting littoral and profundal habitats and foraging resources. The same pattern of parallel divergence was found in all three lakes, suggesting similar natural selection pressures driving and/or maintaining the divergence. The two levels of divergence (a clear and robust benthic – pelagic and a more subtle littoral – profundal divergence) observed in this study apparently represent different stages in the process of ecological speciation.

Invader population speeds up life history during colonization

We explore the long-term developments in population biology and life history during the invasion and establishment of the fish species vendace Coregonus albula in a subarctic watercourse by comparing life-history traits and molecular genetic estimates between the source and the colonist population. The two populations exhibited highly contrasting life-history strategies. Relative to the source population, the colonist population was characterized by slower somatic growth rates, earlier sexual maturation at smaller individual size, higher mortality rates and a shorter life span. The two populations could also be significantly discriminated by the genetic markers. Limited founder effects were detected from heterozygote deficit and reduced allelic richness in the colonist population, but both populations were associated with relatively high genetic diversity. The study reveals that the invasion into a new environment induced large changes in life-history strategy, with typical r-selected traits being more prominent in the colonist than in the source population. We discuss the mechanisms that may explain the observed life-history differences between the source and the colonist population, and argue that the accelerated life history of the colonist population represents an adaptive pioneer strategy aimed at fast population increase during colonization and establishment.

The presence and quantification of splenic ice in the McMurdo Sound Notothenioid fish, Pagothenia borchgrevinki (Boulenger, 1902)

Survival of some polar fishes is associated with high levels of circulating antifreeze glycoproteins (AFGPs). AFGP prevent ice growth giving rise to thermal hysteresis. The inhibiting action of AFGPs implies that polar fish contain ice to which AFGPs adsorb. Cryopelagic Pagothenia borchgrevinki, inhabiting the ice-laden waters of McMurdo Sound, Antarctica, were assayed for ice and ice was found on skin, gills, in the intestine, and in the spleen. Two methods used to assess the number of ice crystals in spleens gave comparable results (12.1+/-1.9 and 22+/-3.8 per spleen). Attempts were made to measure the rate of uptake of ice by P. borchgrevinki held in cages immediately beneath the sub-ice platelet layer in McMurdo Sound; uptake was sporadic. Introduction of ice into fish by spray freezing a small patch of the integument resulted in detection of splenic ice after 1h, illustrating that a mechanism exists for ice transport from the periphery to the spleen. Splenic ice did not seem to be eliminated from fish held in ice-free water at -1.6 degrees C for approximately two months. The relatively small number of splenic ice crystals and the slow rate of ice uptake suggest efficient ice barriers exist in P. borchgrevinki.

Anthropogenic hybridization between endangered migratory and commercially harvested stationary whitefish taxa (Coregonus spp.)

Natural hybridization plays a key role in the process of speciation. However, anthropogenic (human induced) hybridization of historically isolated taxa raises conservation issues. Due to weak barriers to gene flow and the presence of endangered taxa, the whitefish species complex is an excellent study system to investigate the consequences of hybridization in conservation. We focused on three naturally reproductively isolated whitefish taxa in Germany: the endangered, anadromous North Sea houting (NSH) and Baltic houting (BH), which were reintroduced after local extinction, and the commercially stocked European whitefish (EW). To evaluate the genetic integrity of each taxon, source and reintroduced populations of NSH and BH, and EW populations were characterized based on two mitochondrial and 17 microsatellite loci. Additionally, we investigated gill raker counts as an adaptive phenotypic trait. Even though clear genetic and phenotypic differentiation confirmed the houtings as separate evolutionarily significant units, admixture analyses revealed an extensive hybrid zone. Hybridizations were introgressive, positively correlated with genetic diversity, and were reflected in the gill raker counts. The BH distribution range showed higher heterogeneity and stronger admixture than the NSH range. Erroneous stocking with non‐native genotypes best explained these patterns, which pose challenges for the conservation of the endangered NSH and BH.

Invasion genetics of vendace (Coregonus albula (L.)) in the Inari-Pasvik watercourse: revealing the origin and expansion pattern of a rapid colonization event

Species invasions can have wide-ranging biological and socio-economic effects and are generally unwanted by legislation. Identification of the source population as well as the ecology and genetics of both the invader population and the receiving community is of crucial importance. The rapid invasion of a small coregonid fish vendace (Coregonus albula) in a major northern European subarctic watercourse has resulted in a labile ecological situation in the receiving community. The ecological impact of the invasion has been thoroughly documented, but the genetics of the invasion remains to be explored. We analyzed the genetic diversity and divergence patterns among the two possible source populations from southern Finnish Lapland and three colonists populations within the Inari-Pasvik watercourse using ten microsatellite loci in order to (i) identify the most likely source of the invasion, (ii) reveal the dispersal pattern and genetic structure of the secondary expansion, and (iii) to investigate whether the initial introduction and the secondary expansion were associated with founder effects. We revealed that repeated translocation of vendace from Lake Sinettäjärvi into a tributary lake of L. Inari in 1964–1966 is the most plausible source for the invasion. Both the initial introduction and the secondary expansion were found not to be associated with significant founder effects. The secondary expansion followed a stepping stone pattern and the source and colonist populations of this expansion have undergone rapid genetic divergence within a period of 15–35 years (ca. 8–17 generations). The rapid divergence may be contributed to lack of gene flow among the source and colonist populations due to the extensive hydroelectric damming in the watercourse. Multiple introductions and substantial genetic variation in combination with the boom-and-bust population development of the species thus likely counteracted the founder effects as well as fueled the rapid establishment and expansion of this species within the Inari-Pasvik watercourse.

Temperature and salinity conditions in a sub-Arctic intertidal spawning habitat for capelin

Abstract Temperature and salinity were logged every 35 min during 52 days in April and May at a well-known spawning beach for capelin (Mallotus villosus) in Balsfjord, northern Norway. Two loggers were located either on or within the gravel of the spawning ground, whereas a reference logger was deployed 1 m below the lowest astronomical tide (LAT). The temperature on the gravel ranged from −5.3 to 26.7°C with an overall mean of 6.2±3.6°C. The diurnal temperature fluctuations (i.e. the difference between the daily maximum and minimum temperature, ▵T) varied between 3.9 and 20.8°C. Sub-zero temperatures were registered neither within the gravel nor at the reference site and the overall temperature for these loggers fluctuated considerably less than on the gravel. The salinity on the surface of the gravel fluctuated markedly (5.2–28.6 psu) and contrasted the salinities registered within the gravel (1.8–6.3 psu) and below LAT (14.0–30.0 psu). The results suggest that beach-spawned capelin eggs have evolved an array of biological adaptations to survive the unpredictable physical conditions of an intertidal habitat.