Social behaviour and plant morphology: a case of extended phenotype in insects?

Some days ago I received a twit from Marleen Roelofs suggesting me a paper published in Nature Communications and related to aphids. The paper, entitled “An insect-induced novel plant phenotype for sustaining social life in a closed system” is extremely intriguing and deals about the evolution of aphids living inside galls.

Gall aphids (in the photo from the Yavapai County Homepage)  represent a primitive insect social society based on the construction of a completely closed gall on a plant and from hundreds to thousands of aphids grow inside this unusual nest and reproduce for several months in isolation.

Due to their diet enriched in sugars, aphids generally need to produce honeydew that is excreted forming a sticky coating on leaves and many gall-forming social aphids have small openings in their galls through which soldier nymphs actively dispose honeydew droplets and other colony wastes. Surprisingly, some gall aphids live within completely closed galls… but why these aphids are not drowned by accumulated honeydew?  This is a good question since it could be expected that the large quantity of honeydew excreted by hundreds of aphids would quickly fill up the closed gall cavity. Furthermore, when the same aphids were placed on an artificial feeding system consisting of a liquid artificial diet sandwiched by Parafilm membranes, a number of honeydew droplets soon appeared around the insects.

Where is honeydew? Mayako Kutsukake and colleagues identified the sophisticated biological solution that aphids evolved to the waste problem in the closed gall system.

The gall-forming insects manipulate the plant growth and morphogenesis for their own sake in a sophisticated manner, thereby inducing elaborate plant structures as ‘extended phenotypes’ of the insects. During their nest construction, the gall inner surface is specialized for absorbing water, whereby honeydew is promptly removed via the plant vascular system. This plant-mediated waste removal is an efficient mechanism of nest cleaning, which can be regarded as ‘extended phenotype’ and ‘indirect social behavior’ of the social aphids , but seems also to be a sort of trade-off between plants and aphids since plants can al least recover a portion of the sugars that aphids have stolen by feeding.  By contrast, no such water absorption was observed for the open galls where honewdew can be eliminated without any problem.

Interestingly, the aphid species examined in this study represent the tribes Nipponaphidini, Hormaphidini and Cerataphidini and the analysis of the complete set of data indicated that water-absorbing closed galls evolved at least twice independently among social aphids.

I found this paper simply amazing since it shows an elegant strategy for social insect colonies to persist for a considerable period in complete isolation. This is not an easy goal since (except for the inactive hibernation period), insects constantly require a large amount of food from the environment and also produce a large amount of wastes to be disposed outside. By contrast, in gall forming aphids, the plant-made nests directly provide a constant and high-quality food supply, a physical barrier against predators and parasites, mitigated environmental stresses and a mechanism for cleaning galls, the latter enabling them to evolve a unique strategy of social living in completely closed galls.

Reference

Kutsukake, M., Meng, X., Katayama, N., Nikoh, N., Shibao, H., & Fukatsu, T. (2012). An insect-induced novel plant phenotype for sustaining social life in a closed system Nature Communications, 3, 1187-1192 DOI: 10.1038/ncomms2187

Read Full Post »

Do plants and insects share the same symbionts?

Looking in some bacterial 16S sequences obtained by some ants I found some bacteria already known in plants.  This is not unusual for members of the insect order Hemiptera since they are small plant feeders with mouthparts adapted for sucking plant sap. During feeding, their stylets penetrate the plant tissue and withdraw plant fluids making hemipteran insects effective vectors of plant pathogens, especially viruses, but also bacteria. But ants?

While working on several hemipteran–symbiont systems, Caspi-Flugera and Zchori-Feina found high similarities between bacterial genes associated with hemipterans and bacterial genes associated with plants, some of the latter referred to as plant pathogens. Therefore, they assume that some bacteria may be shared by hemipterans and plants, first evolving a symbiont of one and later, via feeding, becoming adapted to the other.

According to Caspi-Flugera and Zchori-Feina: “One possible explanation for the identity in gene sequences of symbionts and endophytes is that the bacterium was first established as an endophyte, later acquired the capacity to be vectored by a hemipteran and, with time, developed the ability to be vertically transmitted (and thus sustained) in the new host. The process of becoming a symbiont demands mutual changes and matching for both the symbiont and the host such that each of the partners will benefit. Such a process can be envisioned because many pathogenic bacteria depend on insect vectors for their horizontal transfer. In return, they may change the plant in ways that make it more attractive for the insect vectors (Weintraub and Beanland, 2006) and eventually, such plant-pathogenic bacteria could become essential for the insect”.

I’m still a bit confuse about what could happen in ants, but the ability of symbiotic bacteria to be transmitted among very diverse species, survive, and develop an array of different lifestyles, is realy amazing having vast implications on virtually all living organisms.

Caspi-Fluger, A., & Zchori-Fein, E. (2010) Do plants and insects share the same symbionts? Israel Journal of Plant Sciences, 58, 113-119 DOI: 10.1560/IJPS.58.2.113

Read Full Post »

Honeydew? Less sweet during night

Aphids feed on plants by piercing them with syringe-like mouth parts and sucking the sap out of the phloem. The primary phloem sap compounds are carbohydrates, whereas amino acids are a relatively minor component of phloem sap and their quantity is normally insufficient for aphid survival. At this regards, more important than the quantity of amino acids available in phloem sap, is the composition of the plant amino acid profile, which is frequently poorly matched to that of aphid’s requirements. Indeed aphids cannot produce ten amino acids (called essential amino acids), the success of aphids, whilst feeding on a phloem sap diet that is frequently impoverished in essential amino acids, is intrinsically related to symbiosis with bacteria, which provides for conversion of surplus non-dietary essential amino acids into forms that are commonly less available in their diet.

Due to the large amount of carbohydrates, aphids are often faced with a surfeit of carbohydrate that results in the egestion of excess carbohydrate as oligosaccharide-rich honeydew from the rectum. It is often incorrectly believed that honeydew is secreted from the cornicles (that are tubes that project from the abdomen of an aphid), whereas cornicles are used to emit pheromones or defensive secretions and not honeydew (as you can see in in the Charles Chien’s photo).

Both the composition of the phloem sap amino acid profile and the quantity of sugars in phloem sap have been shown to affect aphid grow and the composition of their honeydew.

As reported in literature, there are diurnal shifts in phloem composition so that there are differences due to high diurnal vs. low night-time sucrose:amino acid ratios. Is there any effect on aphid grow? Can seasonal and diurnal change in plant physiology influence the performance in phloem sap feeding insects, such as aphids?

In a recent paper,  Taylor S. and colleagues reported in Entomologia Experimentalis et Applicata that the amount of honeydew produced by the aphids Macrosiphum euphorbiae and Myzus persicae tended to be higher during the daytime than at night the difference between mean values for daylight vs. night-time honeydew production increased 1.9-fold for Ma. euphorbiae and 2.6-fold for My. persicae. On the contrary, there were no statistically significant effects due to plant age, or interactions between plant age and time of day, for honeydew production by either aphid species. Taylor et al. also assessed a reduction in honeydew dry mass production overnight that is consistent with a reduction in dietary sucrose concentrations experienced by aphids during this period, together with a night-time decline in both phloem sap sucrose concentrations and aphid feeding.

Aphid honeydew composition may therefore vary during day and night making ants more happy of a diurnal sweet meal!!

Reference
Taylor, S., Parker, W., & Douglas, A. (2012). Patterns in aphid honeydew production parallel diurnal shifts in phloem sap composition Entomologia Experimentalis et Applicata, 142 (2), 121-129 DOI: 10.1111/j.1570-7458.2011.01206.x

Read Full Post »