| In the Holometabola, the larvae have different morphological characteristics and feeding habits from the imagines. The holometabolous larvae and imagines occupy distinct ecological niches and avoid resource competition, making the Holometabola become the most successful clade of animals. However, the evolutionary origin of the holometabolous larvae is a long-standing and controversial issue, which has not yet been satisfactorily resolved. The visual organs of insects include compound eyes, dorsal ocelli, and stemmata. The compound eyes and dorsal ocelli are present in most imaginal insects and the nymphs of the hemimetabolous insects, whereas the stemmata exist only in the larvae of the holometabolous insects. Due to highly structural complexity and evolutionary conservation, the visual organs are often used as prominent models for the research on morphology, molecular genetics, phylogenetics, and evolution of traits. Studies on the evolutionary relationships among compound eyes, dorsal ocelli, and stemmata can help explore the evolutionary origin of the holometabolous larvae.Mecoptera are unique in the Holometabola in that their larvae possess a pair of compound eyes instead of stemmata, in addition that the larval Bittacidae have a dorsal ocellus, indicating the Mecoptera is the crucial link between the Holometabola and Hemimetabola. The compound eyes and dorsal ocellus of the larval Mecoptera are unique ideal materials for uncovering the evolutionary relationships among compound eyes, dorsal ocelli, and stemmata and for exploring the evolutionary origin of the holometabolous larvae.We used light and electron microscopy technologies to compare the morphology and structure of the visual organs of the larval and imaginal Mecoptera. The main results are as follows: The compound eyes of the larvae and imagines are apposition eyes. Each ommatidium consists of a laminated cornea, a quartered eucone crystalline cone, eight retinula cells, two primary pigment cells, and several secondary pigment cells. In the imaginal ommatidia, these retinula cells(R1–R8) are arranged in a “7 + 1” mode that seven retinula cells(R1–R7) extend from the crystalline cone end to the basement membrane, whereas the remaining retinula cell(R8) is located near the basement membrane. The imaginal rhabdom is of fused type and assumes a rod-like shape. The distal part of the rhabdom connects with the end of crystalline cone and is composed of the rhabdomeres of seven retinula cells(R1–R7). At the proximal level, one of seven retinula cells(R7) no longer contributes the microvilli of its rhabdomere to the fused rhabdom, but moves toward the periphery of ommatidia. Instead, the basal retinula cell(R8) contributes its rhabdomere to the fused rhabdom. Thus the proximal part of rhabdom is also formed by the rhabdomeres of seven retinula cells(R1–R6, and R8).In the ommatidia of the larval Mecoptera, the retinula cells(R1–R8) are arranged in a “4 + 4” mode that four distal retinula cells(DRC, 1–4) extend from the crystalline cone end to the basement membrane, whereas the remaining four proximal retinula cells(PRC, 5–8) are located in the proximal part of ommatidia. The larval rhabdom assumes a funnel shape, and its distal part surrounds the basal surface of the crystalline cone. In the ommatidia of the larval Panorpidae, the distal part of the rhabdom is formed by the rhabdomeres of four distal retinula cells(DRC, 1–4). Proximally these distal retinula cells do not form their rhabdomeres but are located at the periphery of ommatidia. The proximal part of the rhabdom is composed of the rhabdomeres of four proximal retinula cells(PRC, 5–8). In the larval Bittacidae, the distal part of the rhabdom is formed by the rhabdomeres of four distal retinula cells(DRC, 1–4), whereas the proximal part contains the rhabdomeres of all retinula cells(R1–R8).The imaginal Mecoptera possess three dorsal ocelli, each of which consists of a cornea, corneagenous cells, retinula cells, and some accessory cells. In the dorsal ocelli of the imaginal Panorpodidae and Panorpidae, the corneagenous cell layers are thick, and the rhabdoms are generally formed by the rhabdomeres of two adjacent retinula cells. In the imaginal Bittacidae, the corneagenous cell layer is relatively thin, and the rhabdom is composed of the rhabdomeres of four retinula cells. A clear zone is present between the corneagenous cell layer and the retinula cells in the dorsal ocelli of the imaginal Panorpodidae but not in those of Panorpidae and Bittacidae.Besides the compound eyes, the larvae of Bittacidae have a dorsal ocellus, which is unique in the Holometabola. The retinula cells of the dorsal ocellus possess numerous irregular-arranged microvilli, which do not form the rhabdomeres or rhabdoms. Thus the dorsal ocellus of the larval Bittacidae may be highly degenerated.We thought that the compound eyes of the larval and imaginal Mecoptera were not homologous organs because the ommatidia of the larval Mecoptera are different in the arrangement of retinula cells and the form of rhabdoms from those of the imagines, in addition that the compound eyes of the larvae degenerate during the pupal stage, when those of the imagines develop from the imaginal discs near the remnants of the larval eyes. We also found that the compound eyes of the larval Mecoptera were similar in structure and development to those of most hemimetabolous insects, indicating that the compound eyes of the larval Mecoptera were likely homologous with those of the hemimetabolous insects.Comparing the compound eyes of the larval Mecoptera with the stemmata of other holometabolous larvae, we thought that the unique compound eyes and dorsal ocellus of the larval Mecoptera are considered as true plesiomorphy of the Holometabola; the stemmata of holometabolous larvae originated from the compound eyes of the hemimetabolous insects and were derived from the ommatidia of the compound eyes. The stemmata of the holometabolous larvae are classified into four basic types, including unicorneal composite eyes, ommatidial-like stemmata, multi-ommatidial stemmata, and Bolwig’s organ of advanced Diptera. The different types of stemmata are present in various holometabolous groups, becoming important characteristics for discussing the phylogenetic relationships among holometabolous groups.In the present study, we first utilized the visual organs to explore the evolutionary origin of the holometabolous larvae and proposed a new “atavistic hypothesis”. We speculated that the holometabolous larvae were likely to originate from the primitive wormlike arthropod ancestors, which are similar to the eruciform larvae of the holometabolous insects. During the evolutionary process, the genes of the ancestors have been reserved as silent genes in the genomes of insects. With the change of the environment, however, these silent genes are re-expressed into the larval forms, which are present in the life history of the Holometabola. In other words, the larvae of the holometabolous insects are likely the result of the re-expression of the ancestral genes, namely “atavistic conditions”. |
PDF Full Text Request