Sentido adaptativo de las agallas inducidas por pulgones de las tribus Fordini y Pemphigini (Aphididae: Eriosomatinae)

Abstract

Plant galls are structures induced de novo by the activity of a gall maker, produced by hypertrophy and hyperplasia phenomena. Their formation and subsequent development is highly dependent on the inducing organism. When the inducing organism induces gall formation, it causes a profound alteration in gene expression in the host plant, resulting in significant changes in its physiology and morphology. Despite the evolutionary interest of this plant insect relationship, the precise mechanisms that trigger gall formation in most gall species are not yet fully understood. However, certain phytohormones, such as indoleacetic acid and other auxins, have been found to play a role in this process. Galls can have beneficial, detrimental or neutral effects on the host plant. Over the decades, various hypotheses have been proposed to explain the adaptive sense of galls, ranging from benefit to the plant to exclusive benefit to the inducing organism. Currently, the most widely accepted hypotheses regarding the adaptive sense of galls include: (i) the nutritional hypothesis, which argues that galls improve the nutritional quality of plant tissues, thus enhancing the reproductive success of the inducer organism; (ii) the enemy hypothesis, which argues that galls possess defence mechanisms that protect the inducer organism against natural predators or parasites; and (iii) the microenvironment hypothesis, which suggests that galls provide a stable environment for the inducer organism, helping it to avoid stress caused by external environmental factors. Nowadays, most of the organisms that induce gall formation are insect species belonging to various orders, such as Hymenoptera, Diptera and Hemiptera. Among the latter, the gall-inducing aphids of the subfamily Eriosomatinae, whose galls are colonial and can harbour from a few tens to thousands of individuals inside. Although there is no broad support for monophyly in this subfamily, it is suggested that the ability to induce gall formation has arisen at least twice independently in this group. In this context, detailed analyses of the galls of this subfamily will provide a deeper understanding of the evolutionary origin of these structures, as well as their adaptive significance. Therefore, the specific objectives of this PhD thesis include: (1) to develop a classification of aphid galls based on histological characteristics; (2) to investigate the dynamic interactions between aphid populations and their relationship with gall development; (3) to confirm the validity of the nutritional hypothesis; and (4) to validate the enemy hypothesis in relation to aphid-induced galls. For this purpose, samples of galls induced by species of Fordini and Pemphigini were collected in the surroundings of Las Médulas and the city of León, respectively. The dimensions of each gall were recorded, as well as the characteristics of the aphid colonies that inhabit them. These galls have subsequently been used to carry out specific studies, including histological, physiological, population and ecological analyses. Based on the histological data collected so far from Fordini and Pemphigini galls, a classification has been carried out which identifies three different types of galls: closed galls, open sac-like galls and open fold-like galls. These galls differ not only in their histological characteristics, but also in biological aspects, such as size of the gall colony, opening mechanisms and waste disposal. The study of hypertrophy and hyperplasia of gall tissues has revealed the importance of phloem development in these structures, as well as the structural role of xylem. From a phylogenetic perspective, it has been confirmed that in Fordini the ability to induce galls arose on a single occasion and that the fold-like galls originate from closed galls. On the other hand, in Pemphigini, both closed galls and open sac-like galls have independent origins from pseudogalls. Analysis of aphid colony and gall development in Fordini species revealed a close interdependence between the two. Both aphid colony and gall growth followed a logistic pattern, and gall development was found to be directly related to colony growth. These results provided insight into the role of the apterous fundatrices in the initial rapid growth of the gall. Findings related to the physiology of mature Forda formicaria galls have provided crucial information on their function as physiological sinks. In addition, evidence has been found suggesting their negative impact on the photosynthetic capacity of the galls and inhibition of the host plant’s defensive systems. The accumulation of soluble sugars, mineral nutrients and potassium, which facilitates the uptake of amino acids by the aphid colony, further supports the nutritional hypothesis. Furthermore, by studying the profile of phytohormones during the early stages of gall development, the specific role of indolacetic acid, isopentenyladenine and isopentenyladenosine in their induction has been elucidated. Finally, it was determined that natural enemies, such as the predator Alophia combustella and the parasitoid Monoctonia pistaciaecola, showed a differential pattern of attack towards Fordini species. These findings suggest the existence of species-specific mechanisms or structures that make them more or less susceptible to attack by natural enemies. These results provide evidences to support the enemy hypothesis in aphid-induced galls. Taken together, these results have established that aphid galls are the result of hypertrophy and hyperplasia of phloem and adjacent tissues. Furthermore, it has been confirmed that the ability to induce gall formation arose once in Fordini and twice in Pemphigini, being the closed galls an evolutionary convergence between the two tribes. Furthermore, both the nutritional hypothesis and the enemy hypothesis have been validated in aphid galls, leading to a better understanding of the adaptive meaning of these galls.