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Amino acid transporter expansions associated with the evolution of obligate endosymbiosis in sap-feeding insects (Hemiptera: sternorrhyncha).

Dahan RA, Duncan RP, Wilson AC, Dávalos LM - BMC Evol. Biol. (2015)

Bottom Line: By applying a series of methods to reconcile gene and species trees, inferring the size of gene families in ancestral lineages, and simulating the process of birth and death in multi-gene families, we uncovered a 10-fold increase in duplication rate in the AAAP family of amino acid transporters within Sternorrhyncha.This gene family expansion was unmatched in other closely related clades lacking endosymbionts that provide essential amino acids.Our findings support the influence of obligate endosymbioses on host genome evolution by both inferring significant expansions of gene families involved in symbiotic interactions, and discovering increases in the rate of duplication associated with multiple emergences of obligate symbiosis in Sternorrhyncha.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY, 11794, USA. romain.a.dahan@gmail.com.

ABSTRACT

Background: Mutualistic obligate endosymbioses shape the evolution of endosymbiont genomes, but their impact on host genomes remains unclear. Insects of the sub-order Sternorrhyncha (Hemiptera) depend on bacterial endosymbionts for essential amino acids present at low abundances in their phloem-based diet. This obligate dependency has been proposed to explain why multiple amino acid transporter genes are maintained in the genomes of the insect hosts. We implemented phylogenetic comparative methods to test whether amino acid transporters have proliferated in sternorrhynchan genomes at rates grater than expected by chance.

Results: By applying a series of methods to reconcile gene and species trees, inferring the size of gene families in ancestral lineages, and simulating the process of birth and death in multi-gene families, we uncovered a 10-fold increase in duplication rate in the AAAP family of amino acid transporters within Sternorrhyncha. This gene family expansion was unmatched in other closely related clades lacking endosymbionts that provide essential amino acids.

Conclusions: Our findings support the influence of obligate endosymbioses on host genome evolution by both inferring significant expansions of gene families involved in symbiotic interactions, and discovering increases in the rate of duplication associated with multiple emergences of obligate symbiosis in Sternorrhyncha.

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Bayesian phylogeny inferred using 20 genes of 13 species. The median posterior likelihood was-160204. Node bars represent the 95% confidence interval for the age of the nodes. The corresponding geological eras are given for reference, and colored according to the Commission for the Geological Map of the World (CGMW), Paris, France.
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Fig1: Bayesian phylogeny inferred using 20 genes of 13 species. The median posterior likelihood was-160204. Node bars represent the 95% confidence interval for the age of the nodes. The corresponding geological eras are given for reference, and colored according to the Commission for the Geological Map of the World (CGMW), Paris, France.

Mentions: Both the maximum likelihood (ML) and Bayesian species phylogenies with 10 partitions recovered Sternorrhyncha as a monophyletic clade within Hemiptera (Table 1, Figure 1, Additional file 1: Figure S1, bootstrap support [bs] = 100, posterior probability [pp] = 0.9995). Auchenorrhyncha (represented by Diceroprocta semicincta) and Heteroptera (represented by Rhodnius prolixus) formed a clade sister to Sternorrhyncha (Figure 1, bs = 100, pp = 0.9955). Psocodea (represented by Pediculus humanus) was sister to Hemiptera in the Bayesian phylogeny, making Paraneoptera monophyletic, although with low support (pp = 0.47, Figure 1). This result was obtained despite the starting ML phylogeny including a paraphyletic Paraneoptera as in [15] (Additional file 1: Figure S2).Table 1


Amino acid transporter expansions associated with the evolution of obligate endosymbiosis in sap-feeding insects (Hemiptera: sternorrhyncha).

Dahan RA, Duncan RP, Wilson AC, Dávalos LM - BMC Evol. Biol. (2015)

Bayesian phylogeny inferred using 20 genes of 13 species. The median posterior likelihood was-160204. Node bars represent the 95% confidence interval for the age of the nodes. The corresponding geological eras are given for reference, and colored according to the Commission for the Geological Map of the World (CGMW), Paris, France.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4374396&req=5

Fig1: Bayesian phylogeny inferred using 20 genes of 13 species. The median posterior likelihood was-160204. Node bars represent the 95% confidence interval for the age of the nodes. The corresponding geological eras are given for reference, and colored according to the Commission for the Geological Map of the World (CGMW), Paris, France.
Mentions: Both the maximum likelihood (ML) and Bayesian species phylogenies with 10 partitions recovered Sternorrhyncha as a monophyletic clade within Hemiptera (Table 1, Figure 1, Additional file 1: Figure S1, bootstrap support [bs] = 100, posterior probability [pp] = 0.9995). Auchenorrhyncha (represented by Diceroprocta semicincta) and Heteroptera (represented by Rhodnius prolixus) formed a clade sister to Sternorrhyncha (Figure 1, bs = 100, pp = 0.9955). Psocodea (represented by Pediculus humanus) was sister to Hemiptera in the Bayesian phylogeny, making Paraneoptera monophyletic, although with low support (pp = 0.47, Figure 1). This result was obtained despite the starting ML phylogeny including a paraphyletic Paraneoptera as in [15] (Additional file 1: Figure S2).Table 1

Bottom Line: By applying a series of methods to reconcile gene and species trees, inferring the size of gene families in ancestral lineages, and simulating the process of birth and death in multi-gene families, we uncovered a 10-fold increase in duplication rate in the AAAP family of amino acid transporters within Sternorrhyncha.This gene family expansion was unmatched in other closely related clades lacking endosymbionts that provide essential amino acids.Our findings support the influence of obligate endosymbioses on host genome evolution by both inferring significant expansions of gene families involved in symbiotic interactions, and discovering increases in the rate of duplication associated with multiple emergences of obligate symbiosis in Sternorrhyncha.

View Article: PubMed Central - PubMed

Affiliation: Department of Ecology and Evolution, State University of New York at Stony Brook, Stony Brook, NY, 11794, USA. romain.a.dahan@gmail.com.

ABSTRACT

Background: Mutualistic obligate endosymbioses shape the evolution of endosymbiont genomes, but their impact on host genomes remains unclear. Insects of the sub-order Sternorrhyncha (Hemiptera) depend on bacterial endosymbionts for essential amino acids present at low abundances in their phloem-based diet. This obligate dependency has been proposed to explain why multiple amino acid transporter genes are maintained in the genomes of the insect hosts. We implemented phylogenetic comparative methods to test whether amino acid transporters have proliferated in sternorrhynchan genomes at rates grater than expected by chance.

Results: By applying a series of methods to reconcile gene and species trees, inferring the size of gene families in ancestral lineages, and simulating the process of birth and death in multi-gene families, we uncovered a 10-fold increase in duplication rate in the AAAP family of amino acid transporters within Sternorrhyncha. This gene family expansion was unmatched in other closely related clades lacking endosymbionts that provide essential amino acids.

Conclusions: Our findings support the influence of obligate endosymbioses on host genome evolution by both inferring significant expansions of gene families involved in symbiotic interactions, and discovering increases in the rate of duplication associated with multiple emergences of obligate symbiosis in Sternorrhyncha.

Show MeSH