Anna Siwertsson

The role of gill raker number variability in adaptive radiation of coregonid fish

Gill raker divergence is a general pattern in adaptive radiations of postglacial fish, but few studies have addressed the adaptive significance of this morphological trait in foraging and eco-evolutionary interactions among predator and prey. Here, a set of subarctic lakes along a diversifying gradient of coregonids was used as the natural setting to explore correlations between gill raker numbers and planktivory as well as the impact of coregonid radiation on zooplankton communities. Results from 19 populations covering most of the total gill raker number gradient of the genus Coregonus, confirm that the number of gill rakers has a central role in determining the foraging ability towards zooplankton prey. Both at the individual and population levels, gill raker number was correlated with pelagic niche use and the size of utilized zooplankton prey. Furthermore, the average body size and the abundance and diversity of the zooplankton community decreased with the increasing diversity of coregonids. We argue that zooplankton feeding leads to an eco-evolutionary feedback loop that may further shape the gill raker morphology since natural selection intensifies under resource competition for depleted prey communities. Eco-evolutionary interactions may thus have a central role creating and maintaining the divergence of coregonid morphs in postglacial lakes.

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.

Temporal stability of niche use exposes sympatric Arctic charr to alternative selection pressures

There is now strong evidence that foraging niche specialisation plays a critical role in the very early stages of resource driven speciation. Here we test critical elements of models defining this process using a known polymorphic population of Arctic charr from subarctic Norway. We test the long-term stability of niche specialisation amongst foraging predators and discuss the possibility that contrasting foraging specialists are exposed to differing selection regimes. Inter-individual foraging niche stability was measured by combining two time-integrated ecological tracers of the foraging niche (each individual’s δ13C and δ15N stable isotope (SI) signatures and their food borne parasite fauna) with a short-term measure of foraging niche use (stomach contents composition). Three dietary subgroups of predators were identified, including zooplankton, gammarid and benthivore specialists foragers. Zooplanktivorous specialists had muscle low in δ 13C, a high abundance of parasites transmitted from pelagic copepods, a smaller head, longer snout and a more slender body-form than gammaridivorous specialist individuals which had muscle more enriched in δ 13C and high abundance of parasites transmitted from benthic Gammarus. Benthivorous individuals were intermediate between the other two foraging groups according to muscle SI-signals (δ13C) and loadings of parasites transmitted from both copepods and Gammarus. The close relationship between subgroups identified by stomach contents, time-integrated tracers of niche use (SI and parasites) and functional trophic morphology (niche adaptations) demonstrate a long-term temporally stable niche use of each individual predator. Differential habitat use and contrasting parasite communities and loadings, show differential exposure to different suites of selection pressures for different foraging specialists. Results also show that individual specialisation in trophic behaviour and thus exposure to different suites of selection pressures are stable over time, and thus provide a platform for disruptive selection to operate within this sympatric system.

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.

Morphological divergence between three Arctic charr morphs – the significance of the deep‐water environment

Morphological divergence was evident among three sympatric morphs of Arctic charr (Salvelinus alpinus (L.)) that are ecologically diverged along the shallow-, deep-water resource axis in a subarctic postglacial lake (Norway). The two deep-water (profundal) spawning morphs, a benthivore (PB-morph) and a piscivore (PP-morph), have evolved under identical abiotic conditions with constant low light and temperature levels in their deep-water habitat, and were morphologically most similar. However, they differed in important head traits (e.g., eye and mouth size) related to their different diet specializations. The small-sized PB-morph had a paedomorphic appearance with a blunt head shape, large eyes, and a deep body shape adapted to their profundal lifestyle feeding on submerged benthos from soft, deep-water sediments. The PP-morph had a robust head, large mouth with numerous teeth, and an elongated body shape strongly related to their piscivorous behavior. The littoral spawning omnivore morph (LO-morph) predominantly utilizes the shallow benthic–pelagic habitat and food resources. Compared to the deep-water morphs, the LO-morph had smaller head relative to body size. The LO-morph exhibited traits typical for both shallow-water benthic feeding (e.g., large body depths and small eyes) and planktivorous feeding in the pelagic habitat (e.g., streamlined body shape and small mouth). The development of morphological differences within the same deep-water habitat for the PB- and PP-morphs highlights the potential of biotic factors and ecological interactions to promote further divergence in the evolution of polymorphism in a tentative incipient speciation process. The diversity of deep-water charr in this study represents a novelty in the Arctic charr polymorphism as a truly deep-water piscivore morph has to our knowledge not been described elsewhere.

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.

Parallel evolution of profundal Arctic charr morphs in two contrasting fish communities

A population of small-sized Arctic charr living their entire life cycle in deep water was recently found in Lake Skogsfjordvatn, Northern Norway. Their phenotype and life history closely resembles the profundal charr morph in another subarctic Norwegian lake, Fjellfrøsvatn. Fjellfrøsvatn has one littoral omnivorous and one small profundal benthivorous (PB) charr morph coexisting with brown trout, whereas Skogsfjordvatn has migratory salmon, trout, charr and eel populations in addition to threespined sticklebacks, resident trout and three resident charr morphs of which one is a large piscivorous profundal morph. We predicted that the small profundal charr morph in Skogsfjordvatn would have a similar trophic niche to the PB-morph in Fjellfrøsvatn and tested this by using stomach content and stable isotope (δ13C and δ15N) analyses. Profundal benthic invertebrates, mainly chironomid larvae, Pisidium sp. mussels and small crustaceans, dominated the diets, and the δ13C and δ15N values indicated almost identical long-term trophic niches of the PB-morphs in both lakes. The prediction was therefore supported. This seems to indicate that the small profundal Arctic charr morphs in these lakes have evolved in parallel, in nearly identical and stable habitat and dietary niches in spite of likely different ecological interactions within the contrasting fish communities.

Divergence and parallelism of parasite infections in Arctic charr morphs from deep and shallow lake habitats

Parasite communities can show large differences in species composition between sympatric host species. Here, we assessed how divergent resource use of polymorphic populations of Arctic charr from two environmentally similar sub-arctic lakes was related to parasite community composition. Large similarities in parasite infections were found for both the reproductively isolated littoral-spawning omnivore LO-morph and the profundal-spawning benthivore PB-morph, reflecting cross-lake similarities in resource use. Furthermore, whereas the PB-morph had the lowest richness and abundance of parasite species in both lakes, a third morph, the profundal-spawning piscivorous PP-morph (one lake only), had the highest parasite richness and accumulated parasites by preying upon fish. These results highlight that host ecology and abiotic factors are important for structuring parasite communities. The dissimilarities in the local parasite species pool between the lakes suggest that stochastic events as well as transmission abilities are involved in structuring the parasite communities. The parallel divergent parasite infections between morphs may form an arena for parasite-mediated selection promoting the incipient speciation process in concert with other factors. The deep-water PB-morphs may avoid parasites by specialising in parasite-poor but low-productive habitats, while the piscivorous PP-morph aggregates infections of detrimental parasites through specialising on energetically rich but generally more heavily parasitised prey.

A specialised cannibalistic Arctic charr morph in the piscivore guild of a subarctic lake

Arctic charr (Salvelinus alpinus) is generally considered an inferior piscivore compared to brown trout (Salmo trutta). However, we demonstrate that a recently described profundal spawning piscivore PP-morph of Arctic charr in a subarctic lake has evolved typical piscivore traits (i.e. large jaws, robust skulls), similar to the co-occurring brown trout but different from the sympatric littoral spawning omnivore LO-morph of Arctic charr. A few large-sized LO-morph, most large-sized PP-morph and trout constitute the piscivore guild, but they differed in prey fish selection. Of the fish-eating deep-water PP-morph, 52% had consumed charr, with a peak during the polar night period (68–80% in November–January). In contrast, the LO-morph and trout were mainly (~90%) inter-specific piscivores eating stickleback. Consequently, the PP-morph was the main charr predator and started to feed on fish at a smaller size and took larger prey relative to their body length than the trout. Stable isotope (δ13C, δ15N) ratios reflect the dietary specialisations in the upper-water (LO-morph, trout) and the deep-water (PP-morph) environments, besides the piscivorous behaviour of the PP-morph and trout. The existence of a shallow-water piscivore (trout) may explain the origin of this PP-morph, taking benefit of underutilised resources of small-sized Arctic charr in the deep-water habitat.

A diagnostic tool for efficient analysis of the population structure, hybridization and conservation status of European whitefish (Coregonus lavaretus (L.)) and vendace (C. albula (L.))

Coregonids constitute one of the most diverse fi sh families in the northern freshwater systems and several species are highly endangered mainly due to anthropogenic pressure. Cost effective and powerful polymerase chain reaction (PCR) microsatellite multiplex assays were established for genetic studies of the population structure, hybridization and conservation status of European whitefi sh (Coregonus lavaretus (L.)) and vendace (C. albula (L.)). An assay containing four PCR multiplexes for co-amplifi cation of 9, 5, 3, and 4 loci was developed for C. lavaretus. Cross-species amplifi cation and rearrangement of the same loci resulted in an assay containing three multiplex reactions of 6, 3, and 4 loci for C. albula. Highly signifi cant pair-wise FST estimates were obtained between C. albula from L. Vaggatem (Norway) and L. Palojärvi (Finland) (FST = 0.301, p < 0.001), between C. lavaretus from L. Skrukkebukta (Norway) and L. Stuorajavri (Norway) (FST = 0.161, p < 0.001), and between morphpairs occurring in the two latter lakes (FST = 0.0135-0.043, p < 0.001). The multiplex assays provided a 100% correct assignment success for discriminating C. lavaretus and C. albula and hence provide a powerful diagnostic tool for the future management of these species.