Do terrestrial ectoparasites disperse with penguins?

Abstract

Dispersal plays a critical role in evolution. Rare long-distance movements can lead to allopatric speciation, whereas frequent movements can facilitate gene flow among disjunct populations and prevent divergence. Dispersal between populations of a species may be difficult to observe directly, and is often inferred from indirect measures such as species occurrence data. Increasingly, however, high resolution genomic data are being used to clarify dispersal and gene flow, in many cases contradicting past assumptions. Islands are excellent model regions for investigating dispersal as they offer replicated habitats with clear geographic boundaries. The sub-Antarctic comprises some of the most geographically isolated island ecosystems in the world, representing an ideal model system for assessing the evolutionary consequences of long-distance dispersal. Strong winds, circumpolar oceanic currents, and extreme climatic cycles are thought to have effectively isolated many sub-Antarctic ecosystems, but a growing body of molecular evidence is beginning to question this rhetoric, with numerous species showing connectivity across the region. Connectivity patterns are, however, complex and are not always predictable from an organism’s inferred dispersal capacity. With environmental change placing unprecedented pressure on isolated ecosystems, there is a pressing need for improved understanding of dispersal processes and population connectivity via genomic analyses of diverse taxa. A number of sub-Antarctic species exhibit gene flow across the region despite lacking active long-distance dispersal capabilities. Brooding, sedentary crustaceans have, for example, rafted on buoyant kelp across thousands of kilometres of open ocean in the sub-Antarctic. The close symbiotic or parasitic relationships that such species maintain with the kelp has resulted in whole communities dispersing together. Indeed, active dispersal is often limited in parasites, which can depend almost entirely on mobile hosts for long-distance movement. A parasite that is unable to travel far with its host would, therefore, be expected to show considerable phylogeographic structure. For example, penguins primarily travel underwater but are hosts to terrestrial ectoparasites (most commonly ticks - Ixodes spp.) when they come ashore to breed. Aquatic host movements may represent a challenge to the survival of penguin ticks, restricting gene flow across their range. This thesis first reviews connectivity patterns and challenges throughout the sub-Antarctic, and then uses a multidisciplinary approach (genomic and physiological data) to test whether some terrestrial parasites (ticks: Acari) are able to travel long distances at sea with their aquatically dispersing hosts (penguins). Results indicate that penguin ticks are physiologically resilient, and may be capable of surviving the conditions faced during aquatic penguin movements between colonies. However, these movements appear to be too sporadic to maintain gene flow across the ticks’ ranges, resulting in broad-scale geographic structure. In contrast, movement on fine scales (within colonies) is inferred – based on lack of genomic structure – to be common, possibly facilitated by social interactions of hosts. These results emphasise the important role of dispersal in isolated regions for range expansion and diversification, and highlight the adaptability of parasites to their hosts’ environments.