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Immune-related functions of the Hivep gene family in East African cichlid fishes.

Diepeveen ET, Roth O, Salzburger W - G3 (Bethesda) (2013)

Bottom Line: We examined a set of new candidate immune genes in East African cichlid fishes.We found signatures of long-term positive selection in four Hivep paralogs and lineage-specific positive selection in Hivep3b in two radiating cichlid lineages.Exposure of the cichlid Astatotilapia burtoni to a vaccination with Vibrio anguillarum bacteria resulted in a positive correlation between immune response parameters and expression levels of three Hivep loci.

View Article: PubMed Central - PubMed

Affiliation: Zoological Institute, University of Basel, 4051 Basel, Switzerland.

ABSTRACT
Immune-related genes are often characterized by adaptive protein evolution. Selection on immune genes can be particularly strong when hosts encounter novel parasites, for instance, after the colonization of a new habitat or upon the exploitation of vacant ecological niches in an adaptive radiation. We examined a set of new candidate immune genes in East African cichlid fishes. More specifically, we studied the signatures of selection in five paralogs of the human immunodeficiency virus type I enhancer-binding protein (Hivep) gene family, tested their involvement in the immune defense, and related our results to explosive speciation and adaptive radiation events in cichlids. We found signatures of long-term positive selection in four Hivep paralogs and lineage-specific positive selection in Hivep3b in two radiating cichlid lineages. Exposure of the cichlid Astatotilapia burtoni to a vaccination with Vibrio anguillarum bacteria resulted in a positive correlation between immune response parameters and expression levels of three Hivep loci. This work provides the first evidence for a role of Hivep paralogs in teleost immune defense and links the signatures of positive selection to host-pathogen interactions within an adaptive radiation.

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Related in: MedlinePlus

Phylogenetic hypotheses based on maximum likelihood for the concatenated dataset and the individual Hivep loci consisting of 40 taxa. (A) Concatenated dataset (13,543 base pairs (bp); best-fitting model of nucleotide substitution: HKY+I+G). Lineages are recovered with maximum support values, whereas relationships within and between lineages are supported with relative high values. The horizontal dotted line separates the five most basal species from the derived lineages: the lamprologines, the eretmodines, and the species belonging to the C-lineage, with the latter marked by the vertical dotted line. (B) Hivep1 (3440 bp; TPM1uf+I+G) well-resolved with all major lineages recovered with high support values. (C) Hivep2a (3143 bp; TIM2+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. All major lineages are monophyletic, except the Cyphotilapiini. (D) Hivep2b (1517 bp; TrN+I+G). Mostly unresolved tree with a basal polytomy, excluding the two outgroup species from all other species. Polytomous relationships were further found for the haplochromine and ectodine lineages. (E) Hivep3a (2142 bp; TPM1uf+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. (F) Hivep3b (3301 bp; HKY+I+G). The lamprologines are positioned within the C-lineage. Black arrows represent the two branches for which ω > 1 was found in the branch-site analyses and their lineage-specific amino acid substitutions. Bootstrap values (PAUP*) and Bayesian posterior probabilities (MrBayes) >50% are shown, respectively, above and below the branches. Cichlid lineage names and a color key for the six cichlid lineages with more than one species included in this study are provided in the gray box in (A). Abbreviations of species names consist of the first three characters of the genus name followed by the first three characters of the species name (Table S1 shows full species names). Branch lengths of T. polylepis were shortened by 50% in all phylogenies and for T. nigrifrons in (E).
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fig1: Phylogenetic hypotheses based on maximum likelihood for the concatenated dataset and the individual Hivep loci consisting of 40 taxa. (A) Concatenated dataset (13,543 base pairs (bp); best-fitting model of nucleotide substitution: HKY+I+G). Lineages are recovered with maximum support values, whereas relationships within and between lineages are supported with relative high values. The horizontal dotted line separates the five most basal species from the derived lineages: the lamprologines, the eretmodines, and the species belonging to the C-lineage, with the latter marked by the vertical dotted line. (B) Hivep1 (3440 bp; TPM1uf+I+G) well-resolved with all major lineages recovered with high support values. (C) Hivep2a (3143 bp; TIM2+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. All major lineages are monophyletic, except the Cyphotilapiini. (D) Hivep2b (1517 bp; TrN+I+G). Mostly unresolved tree with a basal polytomy, excluding the two outgroup species from all other species. Polytomous relationships were further found for the haplochromine and ectodine lineages. (E) Hivep3a (2142 bp; TPM1uf+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. (F) Hivep3b (3301 bp; HKY+I+G). The lamprologines are positioned within the C-lineage. Black arrows represent the two branches for which ω > 1 was found in the branch-site analyses and their lineage-specific amino acid substitutions. Bootstrap values (PAUP*) and Bayesian posterior probabilities (MrBayes) >50% are shown, respectively, above and below the branches. Cichlid lineage names and a color key for the six cichlid lineages with more than one species included in this study are provided in the gray box in (A). Abbreviations of species names consist of the first three characters of the genus name followed by the first three characters of the species name (Table S1 shows full species names). Branch lengths of T. polylepis were shortened by 50% in all phylogenies and for T. nigrifrons in (E).

Mentions: To examine the molecular evolutionary history of the Hivep paralogs, we performed maximum likelihood and Bayesian Inference phylogenetic analyses based on the total sequenced region per locus, and the concatenated dataset including all loci. The phylogenetic topologies of the obtained partial cichlid Hivep gene sequences and the concatenated dataset of 13.5 kb are displayed in Figure 1, A–F. Generally, the observed topologies of the gene trees, and the concatenated tree in particular, correspond with the available species trees (Salzburger et al. 2002; Takahashi 2003; Salzburger and Meyer 2004; Clabaut et al. 2005; Salzburger et al. 2005; Muschick et al. 2012), with T. polylepis, O. tanganicae, B. graueri, B. microlepis, and T. nigrifrons as most basal species, followed by the Lamprologini, the Eretmodini, and the species belonging to the "C-lineage" (Salzburger et al. 2002; Clabaut et al. 2005; Day et al. 2008) (Figure 1). As previously observed (Diepeveen and Salzburger 2011), E. cyanostictus was found at a different position within the C-lineage, whereas this species has been commonly resolved outside the C-lineage in previous studies (Salzburger et al. 2002; Clabaut et al. 2005; Day et al. 2008). Also, the relationships between the individual lineages of the C-lineage altered between the individual gene trees. Long branches were observed for T. polylepis, the lamprologines, individual lamprologine species, different branches within the ectodines in several gene trees, and for the haplochromines in Hivep2b and T. nigrifrons in the Hivep3a gene tree.


Immune-related functions of the Hivep gene family in East African cichlid fishes.

Diepeveen ET, Roth O, Salzburger W - G3 (Bethesda) (2013)

Phylogenetic hypotheses based on maximum likelihood for the concatenated dataset and the individual Hivep loci consisting of 40 taxa. (A) Concatenated dataset (13,543 base pairs (bp); best-fitting model of nucleotide substitution: HKY+I+G). Lineages are recovered with maximum support values, whereas relationships within and between lineages are supported with relative high values. The horizontal dotted line separates the five most basal species from the derived lineages: the lamprologines, the eretmodines, and the species belonging to the C-lineage, with the latter marked by the vertical dotted line. (B) Hivep1 (3440 bp; TPM1uf+I+G) well-resolved with all major lineages recovered with high support values. (C) Hivep2a (3143 bp; TIM2+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. All major lineages are monophyletic, except the Cyphotilapiini. (D) Hivep2b (1517 bp; TrN+I+G). Mostly unresolved tree with a basal polytomy, excluding the two outgroup species from all other species. Polytomous relationships were further found for the haplochromine and ectodine lineages. (E) Hivep3a (2142 bp; TPM1uf+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. (F) Hivep3b (3301 bp; HKY+I+G). The lamprologines are positioned within the C-lineage. Black arrows represent the two branches for which ω > 1 was found in the branch-site analyses and their lineage-specific amino acid substitutions. Bootstrap values (PAUP*) and Bayesian posterior probabilities (MrBayes) >50% are shown, respectively, above and below the branches. Cichlid lineage names and a color key for the six cichlid lineages with more than one species included in this study are provided in the gray box in (A). Abbreviations of species names consist of the first three characters of the genus name followed by the first three characters of the species name (Table S1 shows full species names). Branch lengths of T. polylepis were shortened by 50% in all phylogenies and for T. nigrifrons in (E).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3852383&req=5

fig1: Phylogenetic hypotheses based on maximum likelihood for the concatenated dataset and the individual Hivep loci consisting of 40 taxa. (A) Concatenated dataset (13,543 base pairs (bp); best-fitting model of nucleotide substitution: HKY+I+G). Lineages are recovered with maximum support values, whereas relationships within and between lineages are supported with relative high values. The horizontal dotted line separates the five most basal species from the derived lineages: the lamprologines, the eretmodines, and the species belonging to the C-lineage, with the latter marked by the vertical dotted line. (B) Hivep1 (3440 bp; TPM1uf+I+G) well-resolved with all major lineages recovered with high support values. (C) Hivep2a (3143 bp; TIM2+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. All major lineages are monophyletic, except the Cyphotilapiini. (D) Hivep2b (1517 bp; TrN+I+G). Mostly unresolved tree with a basal polytomy, excluding the two outgroup species from all other species. Polytomous relationships were further found for the haplochromine and ectodine lineages. (E) Hivep3a (2142 bp; TPM1uf+G). The lamprologines plus the five most basal species are found basal of the C-lineage plus Eretmodini. (F) Hivep3b (3301 bp; HKY+I+G). The lamprologines are positioned within the C-lineage. Black arrows represent the two branches for which ω > 1 was found in the branch-site analyses and their lineage-specific amino acid substitutions. Bootstrap values (PAUP*) and Bayesian posterior probabilities (MrBayes) >50% are shown, respectively, above and below the branches. Cichlid lineage names and a color key for the six cichlid lineages with more than one species included in this study are provided in the gray box in (A). Abbreviations of species names consist of the first three characters of the genus name followed by the first three characters of the species name (Table S1 shows full species names). Branch lengths of T. polylepis were shortened by 50% in all phylogenies and for T. nigrifrons in (E).
Mentions: To examine the molecular evolutionary history of the Hivep paralogs, we performed maximum likelihood and Bayesian Inference phylogenetic analyses based on the total sequenced region per locus, and the concatenated dataset including all loci. The phylogenetic topologies of the obtained partial cichlid Hivep gene sequences and the concatenated dataset of 13.5 kb are displayed in Figure 1, A–F. Generally, the observed topologies of the gene trees, and the concatenated tree in particular, correspond with the available species trees (Salzburger et al. 2002; Takahashi 2003; Salzburger and Meyer 2004; Clabaut et al. 2005; Salzburger et al. 2005; Muschick et al. 2012), with T. polylepis, O. tanganicae, B. graueri, B. microlepis, and T. nigrifrons as most basal species, followed by the Lamprologini, the Eretmodini, and the species belonging to the "C-lineage" (Salzburger et al. 2002; Clabaut et al. 2005; Day et al. 2008) (Figure 1). As previously observed (Diepeveen and Salzburger 2011), E. cyanostictus was found at a different position within the C-lineage, whereas this species has been commonly resolved outside the C-lineage in previous studies (Salzburger et al. 2002; Clabaut et al. 2005; Day et al. 2008). Also, the relationships between the individual lineages of the C-lineage altered between the individual gene trees. Long branches were observed for T. polylepis, the lamprologines, individual lamprologine species, different branches within the ectodines in several gene trees, and for the haplochromines in Hivep2b and T. nigrifrons in the Hivep3a gene tree.

Bottom Line: We examined a set of new candidate immune genes in East African cichlid fishes.We found signatures of long-term positive selection in four Hivep paralogs and lineage-specific positive selection in Hivep3b in two radiating cichlid lineages.Exposure of the cichlid Astatotilapia burtoni to a vaccination with Vibrio anguillarum bacteria resulted in a positive correlation between immune response parameters and expression levels of three Hivep loci.

View Article: PubMed Central - PubMed

Affiliation: Zoological Institute, University of Basel, 4051 Basel, Switzerland.

ABSTRACT
Immune-related genes are often characterized by adaptive protein evolution. Selection on immune genes can be particularly strong when hosts encounter novel parasites, for instance, after the colonization of a new habitat or upon the exploitation of vacant ecological niches in an adaptive radiation. We examined a set of new candidate immune genes in East African cichlid fishes. More specifically, we studied the signatures of selection in five paralogs of the human immunodeficiency virus type I enhancer-binding protein (Hivep) gene family, tested their involvement in the immune defense, and related our results to explosive speciation and adaptive radiation events in cichlids. We found signatures of long-term positive selection in four Hivep paralogs and lineage-specific positive selection in Hivep3b in two radiating cichlid lineages. Exposure of the cichlid Astatotilapia burtoni to a vaccination with Vibrio anguillarum bacteria resulted in a positive correlation between immune response parameters and expression levels of three Hivep loci. This work provides the first evidence for a role of Hivep paralogs in teleost immune defense and links the signatures of positive selection to host-pathogen interactions within an adaptive radiation.

Show MeSH
Related in: MedlinePlus