Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

Guðbrandsson, Jóhannes; Kapralova, Kalina H.; Franzdóttir, Sigríður Rut; Bergsveinsdóttir, Þóra Margrét; Hafstað, Völundur; Jónsson, Zophonı́as O.; Snorrason, Sigurður S.; Pálsson, Arnar

doi:10.1101/489104

Cited by 7 publications

(14 citation statements)

References 134 publications

(145 reference statements)

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“…Recent empirical studies for example report relatively conserved patterns of trait covariances among geographically separated populations, which potentially limit their divergence [81,83]. Our results support these observations to some extent because the two morphs (which are entirely sympatric but present genetic signatures of reproductive isolation [46,47]) differed in their correlation of growth traits across developmental stages, and overall appeared to have evolved only subtle differences in their phenotypic covariance structure. While some differences in trait correlations were observed between the two morphs, their hybrids sometimes showed correlations falling outside of the range of values of the pure-bred offspring, which could be interpreted as extreme characters, just like transgressive separate traits usually studied in the context of speciation.…”

Section: Discussionsupporting

confidence: 84%

“…Using multivariate phenotypic data on morphology, behaviour and ontogeny, and considering different developmental stages, we characterized phenotypic variations among two of the four sympatric morphs of Arctic charr ( Salvelinus alpinus ) from lake Thingvallavatn, Iceland, and of their hybrids. These morphs are the small-benthic (SB) and the planktivorous charr (PL), which constitute two genetically differentiated populations [45–47] and differ in head and body shape, habitat use, diet, life-history and parasites [48–50]. The SB charr live in the interstitial spaces of a lava matrix forming the stony littoral zone of the lake, where they forage on benthic invertebrates.…”

Section: Introductionmentioning

confidence: 99%

“…Previous studies already indicate that the PL and the SB charr have evolved genetically based differences in their embryonic growth [49], craniofacial development [52,53], and foraging strategy [54]. The two morphs overlap in their spawning time and places [55] but recent estimates of gene flow indicate substantial reproductive isolation [46,47]. Fertile hybrids (at least of the generation F 1 ) can however easily be produced in laboratory.…”

Section: Introductionmentioning

confidence: 99%

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Multivariate distributions of behavioural, morphological, and ontogenetic traits in hybrids bring new insights into the divergence of sympatric Arctic charr morphs

Horta-Lacueva

Snorrason

Morrissey

et al. 2020

Preprint

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Studying the development of fitness related traits in hybrids from populations diverging in sympatry is a fundamental approach to understand the processes of speciation. However, such traits are often affected by covariance structures that complicate the comprehension of these processes, especially because the interactive relationships between traits of different nature (e.g. morphology, behaviour, life-history) remain largely unknown in this context. In a common garden setup, we conducted an extensive examination of phenotypic traits suspected to be involved in the divergence of two recently evolved morphs of Arctic charr (Salvelinus alpinus), and investigated the consequences of potential patterns of trait covariance on the phenotype of their hybrids. We observed differences among morphs in overall phenotypic variance and in trait correlations. Phenotypic contrainsts also tended to be reduced in the hybrids, which corroborates the narrative of hybridization facilitating adaptive divergence by relaxing trait covariance. However, the hybrids were associated with reduced phenotypic variance at different scales (i.e. at the scale of the entire P matrix and in different parts of the multivariate space), and we identified stronger correlations between several ontogenetic and morphological traits in the hybrids than in both morphs . These findings suggest a limited potential for hybridization to generate phenotypic novelty, and emphasise the need for multivariate approaches conciliating ontogenetic, morphological and behavioural processes to study the processes of adaptive divergence and speciation.

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Section: Discussionsupporting

confidence: 84%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Multivariate distributions of behavioural, morphological, and ontogenetic traits in hybrids bring new insights into the divergence of sympatric Arctic charr morphs

Horta-Lacueva

Snorrason

Morrissey

et al. 2020

Preprint

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“…Barring a full contrast of the four morphs with regard to mtDNA, there seems to be no strong differentiation in mtDNA among morphs in this lake. However, Lake Thingvallavatn is indeed one of the best Arctic charr systems studied worldwide and two studies by Gudbrandsson et al [144, 145] reveal presence of significant development transcriptomic gene expression differences among the four sympatric morphs, suggesting extensive genetic divergence among sympatric morphs. Gudbrandsson et al [144, 145] also discuss an alternative hypothesis of whether or not the piscivore morph exists as one genetic cluster, if it has recently diverged under asymmetric gene flow from other morphs, or if it is an inducible morph due to threshold values in growth before becoming a piscivore.…”

Section: Discussionmentioning

confidence: 99%

“…Thus, a multi-method based eco-evo-devo approach with ecological, morphological and life history studies [146], and state of the art genomics as performed in Lake Tingvallavatn [e.g. 144, 145], seem to be a good avenue, as well as the methods applied in Jacobs et al [23] contrasting two independent replicate lineage radiations of the Arctic charr.…”

Section: Discussionmentioning

confidence: 99%

“And if you gaze long into an abyss, the abyss gazes also into thee”: four morphs of Arctic charr adapting to a depth-gradient in Lake Tinnsjøen

Østbye

Hassve

Peris

et al. 2019

Preprint

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AbstractBackgroundThe origin of species is a central topic in biology aiming at understanding mechanisms, level and rate of diversification. Ecological speciation is an important driver in adaptive radiation during post-glacial intra-lacustrine niche diversification in fishes. The Arctic charr Salvelinus alpinus L. species complex in the Northern hemisphere freshwater systems display huge morphological and life history divergence in lakes with one or several morphs present, thus offering a unique opportunity to address ongoing speciation mechanisms.We studied Arctic charr in Lake Tinnsjøen by fishing in four nominal lake habitats (pelagial, littoral, shallow-moderate profundal, and deep-profundal habitats) down to 350 meters depth. Research topics addressed were; (1) to illuminate Holarctic phylogeography and lineages colonizing Lake Tinnsjøen, (2) to estimate reproductive isolation of morphs or fish using unbiased methods, and (3) to document eco-morphological and life history trait divergence. Also, we compared Lake Tinnsjøen with four Norwegian outgroup populations of Arctic charr.ResultsFour field-assigned morphs were identified in Lake Tinnsjøen; the planktivore morph in all habitats except deep-profundal, the dwarf morph in shallow-moderate profundal, the piscivore morph in shallow-moderate profundal (less in littoral and deep-profundal), and an undescribed new morph – the abyssal morph in the deep-profundal only. The morphs displayed extensive life history variation based on age and size patterns. A moderate to high concordance was observed between field-assigned morphs and four unbiased genetic clusters obtained from microsatellite variation. MtDNA suggested the occurrence of two minor endemic clades in Lake Tinnsjøen likely originating from one widespread colonizing clade in the Holarctic. All morphs were genetically differentiated at microsatellites (FST: 0.12-0.20; with some ongoing gene flow among morphs, and for most mtDNA comparisons (FST: 0.04-0.38). Analyses of Norwegian outgroup lakes implied colonization from a river system below Lake Tinnsjøen.ConclusionOur findings suggest post-glacial adaptive radiation of one colonizing mtDNA lineage with divergent niche specialization along a depth-temperature-productivity-pressure gradient. Concordance between reproductive isolation and the realized habitat of the morphs imply that ecological speciation may be the mechanism of divergence. Particularly novel is the extensive morph diversification with depth into the often unexplored deep-water profundal habitat, suggesting we may have systematically underestimated biodiversity present in lakes.

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The interaction of resource use and gene flow on the phenotypic divergence of benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)

Brachmann

Parsons

Skúlason

et al. 2021

Ecology and Evolution

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Conceptual models of adaptive divergence and ecological speciation in sympatry predict differential resource use, phenotype–environment correlations, and reduced gene flow among diverging phenotypes. While these predictions have been assessed in past studies, connections among them have rarely been assessed collectively. We examined relationships among phenotypic, ecological, and genetic variation in Arctic charr ( Salvelinus alpinus ) from six Icelandic localities that have undergone varying degrees of divergence into sympatric benthic and pelagic morphs. We characterized morphological variation with geometric morphometrics, tested for differential resource use between morphs using stable isotopes, and inferred the amount of gene flow from single nucleotide polymorphisms. Analysis of stable isotopic signatures indicated that sympatric morphs showed similar difference in resource use across populations, likely arising from the common utilization of niche space within each population. Carbon isotopic signature was also a significant predictor of individual variation in body shape and size, suggesting that variation in benthic and pelagic resource use is associated with phenotypic variation. The estimated percentage of hybrids between sympatric morphs varied across populations (from 0% to 15.6%) but the majority of fish had genotypes (ancestry coefficients) characteristic of pure morphs. Despite evidence of reduced gene flow between sympatric morphs, we did not detect the expected negative relationship between divergence in resource use and gene flow. Three lakes showed the expected pattern, but morphs in the fourth showed no detectable hybridization and had relatively low differences in resource use between them. This coupled with the finding that resource use and genetic differentiation had differential effects on body shape variation across populations suggests that reproductive isolation maintains phenotypic divergence between benthic and pelagic morphs when the effects of resource use are relatively low. Our ability to assess relationships between phenotype, ecology, and genetics deepens our understanding of the processes underlying adaptive divergence in sympatry.

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Extensive genetic differentiation between recently evolved sympatric Arctic charr morphs

Cited by 7 publications

References 134 publications

Multivariate distributions of behavioural, morphological, and ontogenetic traits in hybrids bring new insights into the divergence of sympatric Arctic charr morphs

Multivariate distributions of behavioural, morphological, and ontogenetic traits in hybrids bring new insights into the divergence of sympatric Arctic charr morphs

“And if you gaze long into an abyss, the abyss gazes also into thee”: four morphs of Arctic charr adapting to a depth-gradient in Lake Tinnsjøen

The interaction of resource use and gene flow on the phenotypic divergence of benthic and pelagic morphs of Icelandic Arctic charr (Salvelinus alpinus)

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