Coadaptación entre Antarctophthirus microchir (Anoplura: Echinophthiriidae) y el lobo marino de un pelo (Otaria flavescens) en Patagonia y sus implicancias en la morfología, dinámica poblacional y ciclo reproductivo del parásito

Paper in Spanish. Spanish abstract attached

Palabras clave: Antarctophthirus microchir, coadaptación, Echinophthiriidae, ectoparásito, lobo marino de un pelo, Otaria flavescens, piojos.

English abstract

This thesis addresses a number of aspects of the co-evolution between the louse Antarctophthirus microchir Trouessart and Neumann, 1888 (Anoplura, Echinophthiriidae) and its host, the South American sea lion, Otaria flavescens (Shaw, 1800). This system shows interesting features given that the Anoplura are of terrestrial origin, and they are adapted to the air environment. However, A. microchir belongs to a family, Echinophthiriidae, which is exclusive to pinnipeds and otters. Amphibious life of the hosts has imposed serious restrictions on the life cycle of the lice. Specifically, lice seem unable to reproduce underwater and must adjust their reproductive events to those of their host. It is considered that, evolutionarily, there has been a close co-adaptation process that varies from species to species depending on the biology of the host. The objective of this thesis was to study this adaptive process, evaluating the morphological and ecological characteristics of A. microchir. These aspects were individually considered in each chapter, working on diverse adaptations of A. microchir to South American sea lions. This study was carried out throughout five consecutive years (2007–2011) in the sea lion rookery of Punta León, Chubut Province, Argentina. Sampling was restricted to pups because reproduction of this louse species is mostly dependent on sea lion pups because pups stay continuously on land for longer periods than any other age group. The first chapter focalizes in the taxonomic revision of the species, which was troubled by the loss of the holotype, the brief original description and the lack of a reliable determination on this host. Adults were redescribed and, for the first time, the three nymphal stages were described. Considering the conservative morphology, and ecological and evolutionary features of sucking lice, we raise the question of whether A. microchir from different sea lion hosts may represent a complex of cryptic species. Then, the population dynamics of the species was studied to determine the constraints of the cycle. Infestation patterns in pups ≤3 days old suggested that the potential for transmission increased from nymphs 1 to adults. Population trends of each instars with pup age, based on standardised values of abundance, were conserved between years, reflecting the basic dynamics of recruitment and reproduction. However, trends based on log-transformed abundances varied significantly between years; apparently, environmental conditions affected growth of lice populations differently each year. Stage-based deterministic models for population growth of A. microchir suggested generation times from 18 to 23 days. Accordingly, only two lice generations might be produced before pups start going to the sea. Shortening the cycle to accommodate a third generation might be risky, whereas a two generation cycle might at least result in larger females producing higher numbers of viable offspring. The following chapters were approached within this framework. The ultra-structure of A. microchir was analyzed by scanning electron microscopy, identifying the morphological adaptations of the species to the marine environment. This technique, used by first time in echinophthiriid nymphs, show many features of these organisms associated to their adaptations to the marine environment, i.e. chaetotaxis pattern, great development of legs, membranous structure of the abdomen. In the final chapters, the ecological aspects related to habitat selection and the pattern of vertical

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transmission was studied. For the first time to an anoplurans louse the habitat selection was described for each stage, which revealed a differential selection among stages. These differences in the pattern of habitat selection would respond to physiological requirements of each process, i.e. oviposition, morphogenesis, hatching or ontogenetic development. Accordingly, it appears that A. microchir would prefer the host’s ventral area for development and copulation and the dorsal area for oviposition. eggs are laid on the dorsal surface; nymphs 1 hatch there and then migrate to the belly, where they develop into adults and copulate; and then ovigerous females return to the dorsal surface. On the one hand, nymphs 1 are characterised by their low locomotory ability; therefore, the fact that they migrate as soon as they hatch suggests a clear pressure leading to microhabitat restriction. On the other hand, the described pattern of microhabitat selection seems to respond to the physiological requirements of each stage, which vary according to the physiological process considered, e.g. oviposition, morphogenesis, hatching and development. Accordingly, it appears that A. microchir would prefer the host’s ventral area for development and copulation and the dorsal area for oviposition. However, the causes of this pattern are not clear, and many factors could be involved. Considering that sea lion pups periodically soak at high tides, and that prolonged immersion and very high humidity are known to be lethal for lice eggs, selecting the dorsal area would be advantageous for oviposition because it dries much faster. Furthermore, because humidity should be retained for longer periods on the ventral surface of the pup, wetter conditions on the sea lion would prevent desiccation of the nymphs in the very arid environment where O. flavescens breeds. Over 60% of 1-day-old pups were already infected with A. microchir, and the recruitment patterns exhibited a curvilinear trend, with a peak of recruitment in 3-days-old pups. Newborn pups harbored more adults, and females, of A. microchir than nymphs and males, respectively, although this pattern of recruitment is not always conserved in older pups. Among nymphs, the lowest recruitment rate was observed in nymphs 1. This pattern could respond to the relative ability of louse to pass from cows onto pups as well as a process of natural selection, favoring transmission of adults, especially females, because they accrue greater fitness within the tight reproductive schedule of A. microchir. The results obtained in this thesis show the long co-evolutionary process between A. microchir and South American sea lions and the close relationship between behaviour and biology of the parasite with its host. Future studies in different species of pinnipeds, will elucidate the evolutionary adaptations of Echinophthirids, analyzing the trade-offs to which they are subjected and the adaptive responses to them.