Reproductive interference occurs when individuals direct sexual behaviours towards other species and this causes a reduction in the fitness of one or both of the participants. While initially considered to be little more than an aberration, reproductive interference is increasingly recognised, not just as a factor in determining species co-existence and community dynamics, but also as an opportunity to further our understanding of sexual selection. In this thesis I investigate the causes and consequences of reproductive interference between several species of true bugs (Order: Hemiptera) in the family Lygaeidae. These species have a polgynandrous mating system, in which both males and females mate multiple times. I found that the interspecific mating attempts often witnessed in these bugs is likely a consequence of this mating system, as potential cues for species discrimination, in the form of cuticular hydrocarbons, are available and can be utilised by the bugs in some contexts. This is further supported by the finding that pre-copulatory selection on factors such as diet and chemical protection are weak in these insects. Furthermore, my work highlights the context-dependant nature of both the fitness costs associated with reproductive interference, and also of the bugs' intra-specific behaviour. When housed in groups, female Lygaeus equestris did not show consistent fitness losses in response to harassment by either conspecific or heterospecific males, despite previous evidence showing that such males inflict costs on both egg production and longevity when interacting one-to-one. This, combined with the finding that male L. equestris alter their mate-guarding behaviour in the presence of other males, highlights the potential of behavioural flexibility to influence the outcome of inter-species interactions, and the importance of context when attempting to measure phenomena such as reproductive interference.

Host plant selection is an important process during the life cycle of lepidopterans, providing ovipositing sites for adults and food resources for the larvae. The processes behind host plant selection have been extensively studied, especially in closely related species in the context of niche separation. Empirical and theoretical studies have shown that multiple processes, such as resource competition, parasitoid avoidance and reproductive interference between interspecific individuals can affect host plant selection, often leading to niche separation. The aim of this study was to create and analyze a mathematical model using the adaptive dynamics techniques, in order to study the evolution of habitat selection. Our model incorporated three processes: Resource competition in the form of density dependent growth, parasitoid attacks and repro- ductive interference in a two species-two habitat system. It was hypothesized that the presence of parasitoids would promote co-existence through top-down control, while reproductive inter- ference would promote niche separation. The results confirmed both hypotheses. The analysis incorporating only the effect of parasitism showed the evolution of habitat separation when parasitoids attacked randomly and the evolution of co-existence in both habitats in the case of switching parasitoids. On the other hand, incorporating reproductive interference promoted the evolution of partial or complete niche separation. The extent of this process was shown to depend on the strength of reproductive interference and the initial habitat choice of the two species. Stronger reproductive interference increased the size of the set of initial conditions leading to the evolution of complete niche separation. The analysis conducted in this study demonstrated the opposing effects of parasitism and reproductive interference on the evolution of habitat selection, promoting co-existence and separation respectively.

Les défis posés par des facteurs biotiques – les interactions avec des compétiteurs, des parasites, etc. – jouent un rôle important dans l’évolution des populations, mais sont souvent difficiles à étudier. Dans cette étude, nous avons utilisé le système biologique Artemia dans les salins d’Aigues-Mortes, France, pour étudier le caractère et l’évolution de plusieurs interactions interspécifiques. Le système est particulièrement bien adapté à cette recherche : il est simple, contenant deux espèces d’Artemia, trois parasites fortement prévalents (un helminthe et deux microsporidies), et des microbiota variés ; et beaucoup des interactions du système ont été nouvellement établies, car une des espèces d’Artemia est invasive. Nous avons étudié deux types d’interactions. Premièrement, la présence et l’évolution de l’interférence reproductive entre les espèces native et invasive d’Artemia. Nous avons trouvé que l’espèce invasive, qui est sexuée, subit une interférence sévère en allocation des sexes en présence de l’espèce native et asexuée, mais pas d’interférence en gardiennage de partenaire. Deuxièmement, l’évolution de la spécialisation de deux parasites microsporidiennes qui infectent les espèces d’Artemia. En nous basant sur des données de terrain, des infections expérimentales, et de l’évolution expérimentale, nous avons investigué l’état, les causes, et les conséquences de la spécialisation des microsporidies. Les résultats démontrent que les microsporidies sont spécialisées dans l’utilisation d’une des espèces d’hôte, même si elles sont capables de compléter leur cycle de vie dans chacun des deux hôtes. Cette spécialisation paraît être imposée par les outils précis nécessaires à l’exploitation de chaque hôte ; dans les hôtes non-spécialistes, ils provoquaient de l’exploitation sous-optimale, de la virulence maladaptative, et de l’immunopathologie. En général, ces études suggèrent que les facteurs biotiques imposent des pressions de sélection fortes sur Artemia, auxquelles elles ne peuvent pas toujours répondre facilement. L’importance des facteurs biotiques dans un système qui est autrement dominé par des conditions abiotiques extrêmes souligne l’importance des interactions interspécifiques dans l’évolution. / The challenges posed by biotic factors – interactions with competitors, parasites, etc. – play a large role in the evolution of populations, but are generally difficult to study. In this work, we used the Artemia system in the hypersaline salterns of Aigues-Mortes, France, to study the character and evolution of several interspecific interactions. The system is eminently suited to such studies: it is simple, containing two Artemia species, three highly prevalent parasites (one helminth and two microsporidians), and various microbiota; and many of its interactions are newly-established, because one of the Artemia species is invasive. We studied two types of interactions. First, the presence and evolution of reproductive interference between the native and invasive Artemia species. We found that the invasive Artemia species, which is sexual, undergoes severe interference in sex allocation when in the presence of the native, asexual Artemia, but no interference in mate guarding. Second, the evolution of parasite specialization in two microsporidian parasites infecting the Artemia species. Using field data, experimental infections, and experimental evolution, we investigated the state, causes, and consequences of specialization in the microsporidians. Results consistently indicated that the microsporidians are specialized for one host species, despite being able to complete their life cycle in either host. This specialization appears to be imposed by the precise toolkits needed to exploit each host species; in the non-specialized hosts, these triggered suboptimal exploitation, maladaptive virulence, and immunopathology. Overall, these studies suggest that the biotic factors acting on Artemia impose strong selection pressures, to which they cannot always respond easily. The importance of biotic factors in a system which is otherwise dominated by extreme abiotic conditions underlines the importance of species interactions in shaping evolution.

京都大学 / 0048 / 新制・課程博士 / 博士(理学) / 甲第22033号 / 理博第4537号 / 新制||理||1652(附属図書館) / 京都大学大学院理学研究科生物科学専攻 / (主査)准教授 森 哲, 教授 沼田 英治, 教授 中務 真人 / 学位規則第4条第1項該当 / Doctor of Science / Kyoto University / DGAM