Evolution and diversity of Arsenophonus endosymbionts in aphids

Endosymbiotic bacteria are important drivers of insect evolutionary ecology, acting both as partners that contribute to host adaptation and as subtle parasites that manipulate host reproduction. Among them, the genus Arsenophonus is emerging as one of the most widespread lineages. Its biology is, however, entirely unknown in most cases, and it is therefore unclear how infections spread through insect populations. Here we examine the incidence and evolutionary history of Arsenophonus in aphid populations from 86 species, characterizing the processes that shape their diversity. We identify aphids as harbouring an important diversity of Arsenophonus strains. Present in 7% of the sampled species, incidence was especially high in the Aphis genus with more than 31% of the infected species. Phylogenetic investigations revealed that these Arseno‐phonus strains do not cluster within an aphid‐specific clade but rather exhibit distinct evolutionary origins showing that they undergo repeated horizontal transfers (HT) between distantly related host species. Their diversity pattern strongly suggests that ecological interactions, such as plant mediation and parasitism, are major drivers for Arsenophonus dispersal, dictating global incidence across insect communities. Notably, plants hosting aphids may be important ecological arenas for global exchange of Arsenophonus, serving as reservoirs for HT.     

Egg deposition patterns of fig pollinating wasps: implications for studies on the stability of the mutualism

1. Fig pollinating wasps (Agaonidae) enter Ficus inflorescences (figs), oviposit in some of the flowers, and pollinate in the process. Each larva completes its development within a single flower. In most cases, an inflorescence entered by a wasp will represent its only egg‐laying site. The mechanisms that prevent pollinating wasps from exploiting all the flowers inside a fig are not understood. In this study, hypotheses about flower use by pollinating fig wasps were tested by investigating egg deposition patterns in three species. 2. Either one or three wasps were introduced into figs. The figs were then harvested. Serial sections allowed assessment of the presence or absence of a wasp egg in a sample of flowers in each fig. The overall proportion of flowers with eggs and the spatial distribution of eggs were then compared in single wasp figs and three foundress figs. 3. In all species, the proportion of flowers with a wasp egg increased with foundress number but less than three‐fold. 4. In all species, at least in single foundress figs, flowers near the fig cavity were more likely to receive a wasp egg than were flowers near the fig wall. 5. In two species, when the number of foundresses was multiplied by three, there was an increase in the use of flowers near the fig wall, while in the third species, the increase was spread evenly among flowers. 6. Factors affecting wasp egg deposition patterns and the potential of investigating such patterns for studying the stability of the mutualism are discussed.     

The functional implications of active and passive pollination in dioecious figs

Fig-pollinating wasps lay their eggs in fig flowers. Some species of fig-pollinating wasps are active pollinators, while others passively transfer pollen. In dioecious fig species, the ovules of male figs produce wasps but no seeds. By observations and experiments on four dioecious Ficus species we show that (i) passive pollinators distribute pollen haphazardly within figs, but fertilization of female flowers in male figs is inhibited. Consequently, wasp larvae will develop in nonfertilized ovules: they cannot benefit from pollination; (ii) active pollinators efficiently fertilize flowers in which they oviposit. Lack of pollination increases larval mortality. Hence, fig pollinators are not obligate seed eaters but ovule gallers. Active pollination has probably evolved as a way to improve progeny nourishment.
Comparison of pollination and oviposition process in male and female figs, suggests that stigma shape and function have coevolved with pollination behaviour, in relation to constraints linked with dioecy.     

Evolutionary history of aphid-plant associations and their role in aphid diversification

Aphids are intimately linked with their host plants that constitute their only food resource and habitat, and thus impose considerable selective pressure on their evolution. It is therefore commonly assumed that host plants have greatly influenced the diversification of aphids. Here, we review what is known about the role of host plant association on aphid speciation by examining both macroevolutionary and population-level studies. Phylogenetic studies conducted at different taxonomic levels show that, as in many phytophagous insect groups, the radiation of angiosperms has probably favoured the major Tertiary diversification of aphids. These studies also highlight many aphid lineages constrained to sets of related host plants, suggesting strong evolutionary commitment in aphids’ host plant choice, but they fail to document cospeciation events between aphid and host lineages. Instead, phylogenies of several aphid genera reveal that divergence events are often accompanied by host shifts, and suggest, without constituting a formal demonstration, that aphid speciation could be a consequence of adaptation to new hosts. Experimental and field studies below the species level support reproductive isolation between host races as partly due to divergent selection by their host plants. Selected traits are mainly feeding performances and life cycle adaptations to plant phenology. Combined with behavioural preference for favourable host species, these divergent adaptations can induce pre- and post-zygotic barriers between host-specialized aphid populations. However, the hypothesis of host-driven speciation is seldom tested formally and must be weighed against overlooked explanations involving geographic isolation and non-ecological reproductive barriers in the process of speciation.     

New data on aphid fauna (Hemiptera,Aphididae) in?Algeria

A survey of aphids was carried out during the period 2008-2011 in different regions of Algeria by collecting and identifying aphids and their host plants. Aphids were collected from 46 host plants. Forty-six species were reported including thirty-six species which were recorded for the first time in this country and thirty species which were recorded for the first time in the Maghreb (North Africa). This study extends the number of known Algerian aphid to 156 species.     

Oviposition strategies, host coercion and the stable exploitation of figs by wasps

A classic example of a mutualism is the one between fig plants (Ficus) and their specialized and obligate pollinating wasps. The wasps deposit eggs in fig ovules, which the larvae then consume. Because the wasps derive their fitness only from consumed seeds, this mutualism can persist only if the wasps are prevented from laying eggs in all ovules. The search for mechanisms that can limit oviposition and stabilize the wasp-seed conflict has spanned more than three decades. We use a simple foraging model, parameterized with data from two Ficus species, to show how fig morphology reduces oviposition rates and helps to resolve the wasp-seed conflict. We also propose additional mechanisms, based on known aspects of fig biology, which can prevent even large numbers of wasps from ovipositing in all ovules. It has been suggested that in mutualistic symbioses, the partner that controls the physical resources, in this case Ficus, ultimately controls the rate at which hosts are converted to visitors, regardless of relative evolutionary rates. Our approach provides a mechanistic implementation of this idea, with potential applications to other mutualisms and to theories of virulence.     

Phylogenetic relationships, historical biogeography and character evolution of fig-pollinating wasps

Nucleotide sequences from the cytochrome oxidase I (COI) gene were used to reconstruct phylogenetic relationships among 15 genera of fig-pollinating wasps. We present evidence supporting broad-level co-cladogenesis with respect to most but not all of the corresponding groups of figs. Using fossil evidence for calibrating a molecular clock for these data, we estimated the origin of the fig-wasp mutualism to have occurred ca. 90 million years ago. The estimated divergence times among the pollinator genera and their current geographical distributions corresponded well with several features of the break-up of the southern continents during the Late Cretaceous period. We then explored the evolutionary trajectories of two characteristics that hold profound consequences for both partners in the mutualism: the breeding system of the host (monoecious or dioecious) and pollination behaviour of the wasp (passive or active). The fig wasp mutualism exhibits extraordinarily long-term evolutionary stability despite clearly identifiable conflicts of interest between the interactors, which are reflected by the very distinct variations found on the basic mutualistic theme.     

Evolutionary lability of a complex life cycle in the aphid genus <Emphasis Type="Italic">Brachycaudus</Emphasis>

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.     

Buchnera has changed flatmate but the repeated replacement of co‐obligate symbionts is not associated with the ecological expansions of their aphid hosts

Symbiotic associations with bacteria have facilitated important evolutionary transitions in insects and resulted in long‐term obligate interactions. Recent evidence suggests that these associations are not always evolutionarily stable and that symbiont replacement, and/or supplementation of an obligate symbiosis by an additional bacterium, has occurred during the history of many insect groups. Yet, the factors favouring one symbiont over another in this evolutionary dynamic are not well understood; progress has been hindered by our incomplete understanding of the distribution of symbionts across phylogenetic and ecological contexts. While many aphids are engaged into an obligate symbiosis with a single Gammaproteobacterium, Buchnera aphidicola, in species of the Lachninae subfamily, this relationship has evolved into a ‘ménage à trois’, in which Buchnera is complemented by a cosymbiont, usually Serratia symbiotica. Using deep sequencing of 16S rRNA bacterial genes from 128 species of Cinara (the most diverse Lachninae genus), we reveal a highly dynamic dual symbiotic system in this aphid lineage. Most species host both Serratia and Buchnera but, in several clades, endosymbionts related to Sodalis, Erwinia or an unnamed member of the Enterobacteriaceae have replaced Serratia. Endosymbiont genome sequences from four aphid species confirm that these coresident symbionts fulfil essential metabolic functions not ensured by Buchnera. We further demonstrate through comparative phylogenetic analyses that cosymbiont replacement is not associated with the adaptation of aphids to new ecological conditions. We propose that symbiont succession was driven by factors intrinsic to the phenomenon of endosymbiosis, such as rapid genome deterioration or competitive interactions between bacteria with similar metabolic capabilities.