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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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Simulations of gene family evolution in Hemiptera. Null distributions of net expansion or contraction, duplications, and losses of two amino acid transporter gene families within Sternorrhyncha from 1000 simulations of a birth-death model of evolution using GenPhyloData [27]. Expansion or contraction was obtained by subtracting the number of losses from the number of duplications detected in Sternorrhyncha in a single replicate. A. Expansion or contraction in APC and D: AAAP in; B. duplications in APC and E: in AAAP; C. losses in APC and F: in AAAP. The thick black lines represent the values inferred using Notung.
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Fig3: Simulations of gene family evolution in Hemiptera. Null distributions of net expansion or contraction, duplications, and losses of two amino acid transporter gene families within Sternorrhyncha from 1000 simulations of a birth-death model of evolution using GenPhyloData [27]. Expansion or contraction was obtained by subtracting the number of losses from the number of duplications detected in Sternorrhyncha in a single replicate. A. Expansion or contraction in APC and D: AAAP in; B. duplications in APC and E: in AAAP; C. losses in APC and F: in AAAP. The thick black lines represent the values inferred using Notung.

Mentions: Relative to other insects, sternorrhynchans had more amino acid transporter paralogs (Figure 2, Table 2). Both the type of analysis and optimization influenced estimates of the history of amino acid transporter gene families. Notung (reconciliation and parsimony) and DupliPhy-ML (gene copy number and ML) inferred large family expansions or contractions toward the tips of the species phylogeny, as well as a large expansion of the AAAP family at the most recent common ancestor (MRCA) of Sternorrhyncha (Figure 2). In contrast, CAFE (gene copy number and ML) favored a model inferring many smaller-scale expansions throughout the clade (Figure 2). Despite analytical differences, all approaches inferred expansions (a net increase in the size of the gene family, obtained by subtracting the number of losses from the number of duplications in the clade, noted k subsequently) of both amino acid transporter gene families in Sternorrhyncha beyond what is expected from the birth-death model (Figure 3, APC [net expansion inferred in all branches of the clade] k = 6, p = 0.002; AAAP k = 8, p < 10-4). Subsequent simulations showed these expansions were the result of more duplications —as opposed to fewer losses— relative to the expectations of a simulated birth-death model (Figure 3). Notung provided the most conservative estimates of the number of duplications and losses in Sternorrhyncha, and we used its results to compare against the simulated distributions (Figure 2).Figure 2


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)

Simulations of gene family evolution in Hemiptera. Null distributions of net expansion or contraction, duplications, and losses of two amino acid transporter gene families within Sternorrhyncha from 1000 simulations of a birth-death model of evolution using GenPhyloData [27]. Expansion or contraction was obtained by subtracting the number of losses from the number of duplications detected in Sternorrhyncha in a single replicate. A. Expansion or contraction in APC and D: AAAP in; B. duplications in APC and E: in AAAP; C. losses in APC and F: in AAAP. The thick black lines represent the values inferred using Notung.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig3: Simulations of gene family evolution in Hemiptera. Null distributions of net expansion or contraction, duplications, and losses of two amino acid transporter gene families within Sternorrhyncha from 1000 simulations of a birth-death model of evolution using GenPhyloData [27]. Expansion or contraction was obtained by subtracting the number of losses from the number of duplications detected in Sternorrhyncha in a single replicate. A. Expansion or contraction in APC and D: AAAP in; B. duplications in APC and E: in AAAP; C. losses in APC and F: in AAAP. The thick black lines represent the values inferred using Notung.
Mentions: Relative to other insects, sternorrhynchans had more amino acid transporter paralogs (Figure 2, Table 2). Both the type of analysis and optimization influenced estimates of the history of amino acid transporter gene families. Notung (reconciliation and parsimony) and DupliPhy-ML (gene copy number and ML) inferred large family expansions or contractions toward the tips of the species phylogeny, as well as a large expansion of the AAAP family at the most recent common ancestor (MRCA) of Sternorrhyncha (Figure 2). In contrast, CAFE (gene copy number and ML) favored a model inferring many smaller-scale expansions throughout the clade (Figure 2). Despite analytical differences, all approaches inferred expansions (a net increase in the size of the gene family, obtained by subtracting the number of losses from the number of duplications in the clade, noted k subsequently) of both amino acid transporter gene families in Sternorrhyncha beyond what is expected from the birth-death model (Figure 3, APC [net expansion inferred in all branches of the clade] k = 6, p = 0.002; AAAP k = 8, p < 10-4). Subsequent simulations showed these expansions were the result of more duplications —as opposed to fewer losses— relative to the expectations of a simulated birth-death model (Figure 3). Notung provided the most conservative estimates of the number of duplications and losses in Sternorrhyncha, and we used its results to compare against the simulated distributions (Figure 2).Figure 2

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
Related in: MedlinePlus