Structural novelties in organ evolution

Research project P 13944 Structural novelties in organ evolution Harald W. KRENN 24.01.2000 The evolution of novel organs is a prime issue in morphology and evolutionary biology. Such morphological innovations often promote diverse changes leading to new form-function relationships emerging from the interactions between functional constraints and adaptations. Extreme modification of basic mouthpart design associated with specialized feeding is exemplified in flower- visiting insects. Notably, the suctorial proboscis of Lepidoptera can be traced back to the ancestral biting/chewing mouthpart type retained in some taxa of primitive Lepidoptera. The great majority Lepidoptera, however, possesses proboscises for sucking up fluids, predon-driantly floral nectar. The evolution of the lepidopteran proboscis may be regarded as a key innovation in higher Lepidoptera, having opened up nectar as a high-energy food source. Although the overall composition of the proboscis and its homology with the maxillary galeae are well-known, next to no studies have yet dealt with the evolution of its single features and their biological role in feeding. In the plesiomorphic condition, the galea is a diminutive part with only few features. Decoupled from its functional context of the biting/chewing mouthparts, the galeae underwent a conspicuous elongation; interlocked, they formed the coilable lepidopteran proboscis. Compared with the paucity of structures in the plesiomorphic galeae, the proboscis features a number of morphological innovations including galeal linking structures, a complexly-textured galea wall, numerous intragaleal muscles and a novel sensillum type. The evolutionary transformation of these features seems to be conditioned either by the novel uncoiling/coiling mechanism of the proboscis, by constraints to fluid-feeding in general, or by adaptations to particular diets. The proposed comparative investigation is scheduled to deal with the functional anatomy of the proboscis and its sensory equipment. This project will be focused on the diversity and evolution of the novel proboscis muscles and the novel sensilla in a phylogenetic context. The results of the comparative anatomical research on the galea musculature shall reveal the plesiomorphic and apomorphic muscle arrangement patterns and * elucitate the origin and the evolutionary pathways of the intragaleal muscles in correlation with the elongation and evolution of new proboscis motility mechanism. The ultrastructural examination of the proboscis sensilla shall * reconstruct the groundplan features of the novel sensillum type, * reveal its evolutionary origin and * clarify the evolution of the sensillum equipment in correspondence with adaptations to food sources and feeding habits. This investigation will require modem histological techniques, comparative electronmicroscopical studies and computer-supported image analysis. Results shall also provide the basics for future physiological and behavioural studies.

The evolution of novel organs is central to morphology and evolutionary biology. Morphological innovations often emerge as interactions between adaptation to new environmental conditions and functional constraints resulting from new form-function relationships. The aim of the 3-year project has been the investigation of the musculature and sensory equipment of insect mouthparts within the phylogenetic context of the Lepidoptera, i.e. the butterflies and moths. Beginning with the ancestral musculature of the maxillae in basal Lepidoptera, the origin, the evolution and functional role of the novel, complex musculature of the proboscis in derived groups could be revealed. The comparative investigation of the sensory structures of the proboscis by electron microscopy generated a hypothesis on the evolutionary origin of the bizarre sensilla on the tip of the proboscis. It concluded that the modifications of these sensilla evolved in context with adaptations to new food sources in particular butterflies. Furthermore, an essential methodological contribution to microanatomical studies of insects was recently published. In a cooperative study we were successful in disclosing the evolutionary origin of a complex new organ which is endowed with its own musculature and sensilla. This new organ arose in the females of yucca moths presumably as a result of the coevolutionary interaction between the pollinating moths and the yucca plant which constitutes the larval food plant. The comparative morphological study of this new mouthpart organ has led to the proposal of a hypothesis for the development of novel organs that might be based on the shift of existing genetic templates to other structures. The mouthparts of Lepidoptera have attained exemplary status in studies on the development and evolution of novel muscle systems considered within a phylogenetic context. The lepidopteran proboscis represents certainly the best investigated model for the functioning of a non-articulated arthropod limb. Furthermore, specializations of the mouthparts have been excellently connected to derived feeding preferences in several studies of ecomorphology and behavior.