Genome duplication and multiple evolutionary origins of complex migratory behavior in Salmonidae

Alexandrou, Markos A.; Swartz, Β. K.; Matzke, Nicholas J.; Oakley, Todd H.

doi:10.1016/j.ympev.2013.07.026

“…Similar analyses at the protein 8/28 ) found a lower proportion with homology, 43% to 55% depending on the database in the two salmonids and other organisms ( Table 2). Even though Arctic charr is considered more closely related to rainbow trout than salmon (Koop et al, 2008;Crête-Lafrenière et al, 2012;Alexandrou et al, 2013) a larger number of transcripts had significant blast hits to salmon. Most likely this reflects the more conservative approach used for annotation of the rainbow trout genome (Berthelot et al, 2014).…”

Section: Resultsmentioning

confidence: 99%

Differential gene expression during early development in recently evolved and sympatric Arctic charr morphs

Guðbrandsson

¹

,

Franzdóttir

²

,

Kristjánsson

³

et al. 2017

Preprint

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Phenotypic differences between closely related taxa or populations can arise through genetic variation or be environmentally induced, in both cases leading to altered transcription of genes during the structural and functional development of the body. Comparative developmental studies of closely related species or variable populations of the same species can help to elucidate the molecular mechanisms related to population divergence and speciation. Studies of Arctic charr (Salvelinus alpinus) and related salmonids have revealed considerable phenotypic variation among populations and in Arctic charr many cases of extensive variation within lakes (resource polymorphism) have been recorded. One example is the four Arctic charr morphs in the ∼10.000 year old Lake Thingvallavatn, which differ in numerous morphological and life history traits. We set out to investigate the molecular and developmental roots of this polymorphism by studying gene expression in embryos of three of the morphs reared in a common garden set-up. We performed RNA-sequencing, de-novo transcriptome assembly and compared gene expression among morphs during a timeframe in early development. Expectedly, developmental time was the predominant explanatory variable. As the data were affected by RNA-degradation, an estimate of 3'-bias was the second most common explanatory variable. Morph, both as a independent variable and as interaction with developmental time, affected the expression of numerous transcripts. The majority of transcripts with significant morph effects separated the limnetic and the benthic morphs. However, gene ontology analyses did not reveal clear functional enrichment of transcripts between groups. Verification via qPCR confirmed differential expression of several genes between the morphs, including regulatory genes such as Arid4a and Tsn. The data are consistent with a scenario where genetic divergence has contributed to differential expression of multiple genes and systems during early development of these sympatric Arctic charr morphs.

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“…The ancestor of all extant salmonids underwent a tetraploidization event (Johnson et al, 1987), according to most recent estimations probably between 80 and 50 mya (Alexandrou et al, 2013). From the 1970ies on (Ohno, 1970b), it has been suspected that the salmonid specific genome duplication event, which preceded the origin of migratory behavior, provided the genetic basis for this evolutionary innovation (Alexandrou et al, 2013).…”

Section: Additional Lineage-specific Wgds Occurred In Salmonids and Smentioning

confidence: 99%

“…From the 1970ies on (Ohno, 1970b), it has been suspected that the salmonid specific genome duplication event, which preceded the origin of migratory behavior, provided the genetic basis for this evolutionary innovation (Alexandrou et al, 2013).…”

Section: Additional Lineage-specific Wgds Occurred In Salmonids and Smentioning

confidence: 99%

See 1 more Smart Citation

Whole-genome duplication in teleost fishes and its evolutionary consequences

Glasauer

¹

,

Neuhauss

²

2014

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Whole-genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, by far the most species-rich vertebrate clade. After initial controversy, there is now solid evidence that such event took place in the common ancestor of all extant teleosts. It is termed teleost-specific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosage selection (preserving genes to maintain dosage balance between interconnected components). Since the frequency of these mechanisms is influenced by the genes' properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massive radiation of teleosts, have been matter of controversial debate. It is evident that gene duplications are crucial for generating complexity and that WGDs provide large amounts of raw material for evolutionary adaptation and innovation. However, it is less clear whether the TS-WGD is directly linked to the evolutionary success of teleosts and their radiation. Recent studies let us conclude that TS-WGD has been important in generating teleost complexity, but that more recent ecological adaptations only marginally related to TS-WGD might have even contributed more to diversification. It is likely, however, that TS-WGD provided teleosts with diversification potential that can become effective much later, such as during phases of environmental change. AbstractWhole genome duplication (WGD) events have shaped the history of many evolutionary lineages. One such duplication has been implicated in the evolution of teleost fishes, the by far most species-rich vertebrate clade. After initial controversy, evidence is now solid that such an event took place in the common ancestor of all extant teleosts, the so-called teleostspecific (TS) WGD. After WGD, duplicate genes have different fates. The most likely outcome is non-functionalization of one duplicate gene due to the lack of selective constraint on preserving both copies of the gene. Mechanisms that act on preservation of duplicates are subfunctionalization (partitioning of ancestral gene functions on the duplicates), neofunctionalization (assigning a novel function to one of the duplicates) and dosageselection (preserving genes to maintain dosage-balance between interconnected components).Since the frequency of these mechanisms is influenced by the gene's properties, there are over-retained classes of genes, such as highly expressed ones and genes involved in neural function. The consequences of the TS-WGD, especially its impact on the massi...

show abstract

“…Similar analyses at the protein ) found a lower proportion with homology, 43% to 55% depending on the database in the two salmonids and other organisms ( Table 2). Even though Arctic charr is considered more closely related to rainbow trout than salmon (Koop et al, 2008;Crête-Lafrenière et al, 2012;Alexandrou et al, 2013) a larger number of transcripts had significant blast hits to salmon. Most likely this reflects the more conservative approach used for annotation of the rainbow trout genome (Berthelot et al, 2014).…”

Section: Resultsmentioning

confidence: 99%

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Supplemental Information 1: The Results of Gene Ontology Analyses of the Transcripts With Significant Expression Difference Bet

0

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Phenotypic differences between closely related taxa or populations can arise through genetic variation or be environmentally induced, in both cases leading to altered transcription of genes during the structural and functional development of the body. Comparative developmental studies of closely related species or variable populations of the same species can help to elucidate the molecular mechanisms related to population divergence and speciation. Studies of Arctic charr (Salvelinus alpinus) and related salmonids have revealed considerable phenotypic variation among populations and in Arctic charr many cases of extensive variation within lakes (resource polymorphism) have been recorded. One example is the four Arctic charr morphs in the ∼10.000 year old Lake Thingvallavatn, which differ in numerous morphological and life history traits. We set out to investigate the molecular and developmental roots of this polymorphism by studying gene expression in embryos of three of the morphs reared in a common garden set-up. We performed RNA-sequencing, de-novo transcriptome assembly and compared gene expression among morphs during a timeframe in early development. Expectedly, developmental time was the predominant explanatory variable. As the data were affected by RNA-degradation, an estimate of 3'-bias was the second most common explanatory variable. Morph, both as a independent variable and as interaction with developmental time, affected the expression of numerous transcripts. The majority of transcripts with significant morph effects separated the limnetic and the benthic morphs. However, gene ontology analyses did not reveal clear functional enrichment of transcripts between groups. Verification via qPCR confirmed differential expression of several genes between the morphs, including regulatory genes such as Arid4a and Tsn. The data are consistent with a scenario where genetic divergence has contributed to differential expression of multiple genes and systems during early development of these sympatric Arctic charr morphs.

show abstract

Genome duplication and multiple evolutionary origins of complex migratory behavior in Salmonidae

Cited by 105 publications

References 90 publications

Differential gene expression during early development in recently evolved and sympatric Arctic charr morphs

Differential gene expression during early development in recently evolved and sympatric Arctic charr morphs

Whole-genome duplication in teleost fishes and its evolutionary consequences

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