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Evolutionary lability of a complex life cycle in the aphid genus Brachycaudus.

Emmanuelle J, Gwenaelle G, Armelle Cd - BMC Evol. Biol. (2010)

Bottom Line: There have been many shifts in feeding behaviour but we found no significant correlation between life cycle changes and changes in diet.Life cycle changes, whether corresponding to the loss or acquisition of a primary host, necessarily promote speciation, by inducing shifts of the reproductive phase on different plants.We suggest that the evolutionary lability of life cycle may have driven speciation events in the Brachycaudus genus.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA, UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro), Campus international de Baillarguet, CS 30016, F-34988 Montferrier-sur-Lez cedex, France. jousseli@supagro.inra.fr

ABSTRACT

Background: Most aphid species complete their life cycle on the same set of host-plant species, but some (heteroecious species) alternate between different hosts, migrating from primary (woody) to secondary (herbaceous) host plants. The evolutionary processes behind the evolution of this complex life cycle have often been debated. One widely accepted scenario is that heteroecy evolved from monoecy on woody host plants. Several shifts towards monoecy on herbaceous plants have subsequently occurred and resulted in the radiation of aphids. Host alternation would have persisted in some cases due to developmental constraints preventing aphids from shifting their entire life cycle to herbaceous hosts (which are thought to be more favourable). According to this scenario, if aphids lose their primary host during evolution they should not regain it. The genus Brachycaudus includes species with all the types of life cycle (monoecy on woody plants, heteroecy, monoecy on herbs). We used this genus to test hypotheses concerning the evolution of life cycles in aphids.

Results: Phylogenetic investigation and character reconstruction suggest that life cycle is evolutionary labile in the genus. Though ancestral character states can be ambiguous depending on optimization methods, all analyses suggest that transitions from monoecy on herbs towards heteroecy have occurred several times. Transitions from heteroecy towards monoecy, are also likely. There have been many shifts in feeding behaviour but we found no significant correlation between life cycle changes and changes in diet.

Conclusions: The transitions from monoecy on herbs towards heteroecy observed in this study go against a widely accepted evolutionary scenario: aphids in the genus Brachycaudus seem to be able to recapture their supposedly ancestral woody host. This suggests that the determinants of host alternation are probably not as complicated as previously thought. Definitive proofs of the lability of life cycle in Brachycaudus will necessitate investigation of these determinants. Life cycle changes, whether corresponding to the loss or acquisition of a primary host, necessarily promote speciation, by inducing shifts of the reproductive phase on different plants. We suggest that the evolutionary lability of life cycle may have driven speciation events in the Brachycaudus genus.

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Species delimitation results. The vertical bars group all specimens identified as belonging to a significant cluster.
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Figure 2: Species delimitation results. The vertical bars group all specimens identified as belonging to a significant cluster.

Mentions: Our sampling initially comprised 29 recognised Brachycaudus species identified on the basis of classical taxonomy and three unidentified specimens. For the Brachycaudus ultrametric tree obtained with Multidivtime, the GMYC model was preferred over the model of uniform branching patterns (2ΔL = 19.67, χ2 test P << 0.0001). This species delimitation method retrieved 27 phylogenetic species of Brachycaudus (Fig. 2). Most species recognized by classical taxonomy were retrieved by our method. However, this method also clustered several species together. B. lateralis (Walker, 1848) and B. cardui (Linnaeus, 1758) specimens were grouped together as a single entity. This suggests that B. lateralis and B. cardui do not form the two species generally defined -- one mostly anholocyclic (without a sexual phase) on Asteraceae and the other alternating between Prunus and plants from several different families (mostly Asteraceae and Boraginaceae) -- but instead form a single species displaying host alternation between Prunus and several plant families. B. lateralis is indeed sometimes treated as a subspecies of B. cardui. All species of the subgenus Appelia other than B. cerinthis also clustered together, even if several specimens from central Asia were included. Brachycaudus (Acaudus) spp. associated with Caryophyllaceae, except B. divaricatae (Shaposhnikov, 1956) and B. klugkisti (Börner, 1942), also formed a single genetic cluster. Specimens identified as B. lami (Koch, 1854) and B. ballotae (Passerini, 1860) were also identified as belonging to a single species. These clustering patterns confirmed our previous findings, based on less extensive specimen and species sampling and fewer DNA markers [23]. The clusters obtained all corresponded to groups of species in which species identification can be difficult and specimens may be assigned to species on the basis of host affiliation or morphological characters subject to intraspecific variation. However, this method detected two clusters within B. helichrysi (Kaltenbach, 1843) and two clusters among the Thuleaphis specimens collected in Kazakhstan that we failed to identify. Two of the Thuleaphis specimens collected on Atraphaxis sp. formed a phylogenetic cluster, and one specimen collected on a Rheum sp. but morphologically different from B. rumexicolens (Patch, 19717) appeared as a separate, differentiated taxon. These two phylogenetic species may correspond to the two new Thuleaphis species reported by Kadyrbekov [26,27].


Evolutionary lability of a complex life cycle in the aphid genus Brachycaudus.

Emmanuelle J, Gwenaelle G, Armelle Cd - BMC Evol. Biol. (2010)

Species delimitation results. The vertical bars group all specimens identified as belonging to a significant cluster.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2958166&req=5

Figure 2: Species delimitation results. The vertical bars group all specimens identified as belonging to a significant cluster.
Mentions: Our sampling initially comprised 29 recognised Brachycaudus species identified on the basis of classical taxonomy and three unidentified specimens. For the Brachycaudus ultrametric tree obtained with Multidivtime, the GMYC model was preferred over the model of uniform branching patterns (2ΔL = 19.67, χ2 test P << 0.0001). This species delimitation method retrieved 27 phylogenetic species of Brachycaudus (Fig. 2). Most species recognized by classical taxonomy were retrieved by our method. However, this method also clustered several species together. B. lateralis (Walker, 1848) and B. cardui (Linnaeus, 1758) specimens were grouped together as a single entity. This suggests that B. lateralis and B. cardui do not form the two species generally defined -- one mostly anholocyclic (without a sexual phase) on Asteraceae and the other alternating between Prunus and plants from several different families (mostly Asteraceae and Boraginaceae) -- but instead form a single species displaying host alternation between Prunus and several plant families. B. lateralis is indeed sometimes treated as a subspecies of B. cardui. All species of the subgenus Appelia other than B. cerinthis also clustered together, even if several specimens from central Asia were included. Brachycaudus (Acaudus) spp. associated with Caryophyllaceae, except B. divaricatae (Shaposhnikov, 1956) and B. klugkisti (Börner, 1942), also formed a single genetic cluster. Specimens identified as B. lami (Koch, 1854) and B. ballotae (Passerini, 1860) were also identified as belonging to a single species. These clustering patterns confirmed our previous findings, based on less extensive specimen and species sampling and fewer DNA markers [23]. The clusters obtained all corresponded to groups of species in which species identification can be difficult and specimens may be assigned to species on the basis of host affiliation or morphological characters subject to intraspecific variation. However, this method detected two clusters within B. helichrysi (Kaltenbach, 1843) and two clusters among the Thuleaphis specimens collected in Kazakhstan that we failed to identify. Two of the Thuleaphis specimens collected on Atraphaxis sp. formed a phylogenetic cluster, and one specimen collected on a Rheum sp. but morphologically different from B. rumexicolens (Patch, 19717) appeared as a separate, differentiated taxon. These two phylogenetic species may correspond to the two new Thuleaphis species reported by Kadyrbekov [26,27].

Bottom Line: There have been many shifts in feeding behaviour but we found no significant correlation between life cycle changes and changes in diet.Life cycle changes, whether corresponding to the loss or acquisition of a primary host, necessarily promote speciation, by inducing shifts of the reproductive phase on different plants.We suggest that the evolutionary lability of life cycle may have driven speciation events in the Brachycaudus genus.

View Article: PubMed Central - HTML - PubMed

Affiliation: INRA, UMR CBGP (INRA/IRD/Cirad/Montpellier SupAgro), Campus international de Baillarguet, CS 30016, F-34988 Montferrier-sur-Lez cedex, France. jousseli@supagro.inra.fr

ABSTRACT

Background: Most aphid species complete their life cycle on the same set of host-plant species, but some (heteroecious species) alternate between different hosts, migrating from primary (woody) to secondary (herbaceous) host plants. The evolutionary processes behind the evolution of this complex life cycle have often been debated. One widely accepted scenario is that heteroecy evolved from monoecy on woody host plants. Several shifts towards monoecy on herbaceous plants have subsequently occurred and resulted in the radiation of aphids. Host alternation would have persisted in some cases due to developmental constraints preventing aphids from shifting their entire life cycle to herbaceous hosts (which are thought to be more favourable). According to this scenario, if aphids lose their primary host during evolution they should not regain it. The genus Brachycaudus includes species with all the types of life cycle (monoecy on woody plants, heteroecy, monoecy on herbs). We used this genus to test hypotheses concerning the evolution of life cycles in aphids.

Results: Phylogenetic investigation and character reconstruction suggest that life cycle is evolutionary labile in the genus. Though ancestral character states can be ambiguous depending on optimization methods, all analyses suggest that transitions from monoecy on herbs towards heteroecy have occurred several times. Transitions from heteroecy towards monoecy, are also likely. There have been many shifts in feeding behaviour but we found no significant correlation between life cycle changes and changes in diet.

Conclusions: The transitions from monoecy on herbs towards heteroecy observed in this study go against a widely accepted evolutionary scenario: aphids in the genus Brachycaudus seem to be able to recapture their supposedly ancestral woody host. This suggests that the determinants of host alternation are probably not as complicated as previously thought. Definitive proofs of the lability of life cycle in Brachycaudus will necessitate investigation of these determinants. Life cycle changes, whether corresponding to the loss or acquisition of a primary host, necessarily promote speciation, by inducing shifts of the reproductive phase on different plants. We suggest that the evolutionary lability of life cycle may have driven speciation events in the Brachycaudus genus.

Show MeSH
Related in: MedlinePlus