Header

UZH-Logo

Maintenance Infos

Optimal Immunity, Reproductive Manipulation, and Dispersal in Host-Parasite Interactions


Brenninger, Franziska Andrea. Optimal Immunity, Reproductive Manipulation, and Dispersal in Host-Parasite Interactions. 2024, University of Zurich, Faculty of Science.

Abstract

Half of all species are estimated to be parasites, making parasitism the most common symbiotic interaction between organisms. To avoid the detrimental effects of parasites, hosts have developed several adaptations to counteract parasitic attacks. These defences involve the development and maintenance of a functional immune system, alongside behavioural tactics to prevent initial contact with parasites (avoidance), fending off infection upon exposure (resistance), or mitigating their harmful effects post-infection (tolerance). In contrast, parasites have evolved various ways to exploit their hosts, while balancing proliferation in the current with transmission to a new host. Intriguingly, some parasites can manipulate host biology to facilitate increased transmission rates. Endosymbionts that live inside their arthropod hosts, for example, are well known to manipulate host reproduction, with potentially severe consequences for host population dynamics. In this thesis, I cover several aspects of host-parasite interactions, by considering optimal resource allocation towards immunity in a host experiencing different levels of sexual selection and parasite impact, the theoretical reasons why reproductive manipulations aid the spread of a parasitic endosymbiont and how dispersal strategies of host and parasite can influence the spread of a vertically transmitted male killing endosymbiont. Continued interactions between host and parasite will shape the functions and strength of a host’s immune defence. Immunocompetence can systematically differ within a species, where one sex produces higher levels of immunity. Ultimate explanations for this sexual dimorphism hypothesize that the sex experiencing higher levels of sexual selection, requires comparatively higher allocation of resources into the production of sexually selected traits to successfully attain fitness, thereby sacrificing immunity. Modelling a tradeoff between investments into reproduction and immunity, I show that parasite abundance and severity can significantly alter optimal immunity investment levels towards trends that can be contrary to what is predicted by the strength of sexual selection alone. While hosts are generally expected to increase investment into immunity when facing more severe or abundant parasites, I find scenarios where immunity investment can become futile, depending on parasite traits and host immune functions. Hosts should not allocate resources towards resistance when infection is unavoidable and instead invest all resources into reproduction making the most of a small lifespan, regardless of the level of sexual selection. Investments into tolerance mechanisms remain beneficial to the host even when parasites are very abundant but should be neglected in case parasites are exceedingly severe. In hosts that are capable of both, allocating investments into immunity remains optimal for host fitness. Thus, when sexes encounter different numbers or severities of parasites, the direction of sexual dimorphism is expected to shift accordingly (chapter II). How a parasite impacts its host can vary depending on host sex, especially when one sex is crucial for parasite transmission. Parasitic endosymbionts transmit almost exclusively vertically from a female host to her offspring, while male hosts represent an evolutionary dead-end to the parasite. To enhance spread through the host population, these endosymbionts evolved conceptually distinct strategies to manipulate host reproduction. I present all cases of reproductive manipulation currently known in arthropod hosts (male killing, feminization, parthenogenesis induction, sex allocation distortion and cytoplasmic incompatibility) and describe their infection dynamics in a unified modelling framework. Using the framework, I compare the ease of spread between endosymbionts using different types of reproductive manipulations and contrast the findings with the incidence of each manipulation across different host species. With the limitation that reports on reproductive manipulations could be biased, there are large discrepancies between how common each manipulation is in natural systems and the model predictions, most likely due to mechanistic constraints, with some manipulations more easily facilitated than others (chapter III). Linking dispersal and parasitic manipulation creates an intriguing mechanism of how parasitic manipulation can indirectly shape behaviour of uninfected hosts. Remaining with endosymbionts that manipulate host reproduction, I use individual based simulations to model the evolution of host dispersal during the spread of a male killing endosymbiont in a spatially structured host population in chapter IV. Since male killing endosymbionts are transmitted vertically from mother to offspring and infected male offspring die, populations can locally run out of males, unless this effect is counteracted by immigrant males. The male killer infection can spread and persist in the host population under intermediate host dispersal patterns. Uninfected males disperse comparatively more due to male-male competition during mating. When exploring a hypothetical scenario in which the male killer can additionally influence its host’s dispersal, I find that infected and uninfected individuals evolve distinct dispersal patterns, where uninfected males and females become philopatric, leading to a shift towards overall female biased dispersal. The selection for divergent dispersal patterns emerges only after parasites become highly abundant in the population. Relating these theoretical results to the natural study system that inspired the model, the African Monarch butterfly Danaus chrysippus and the male killing endosymbiont Spiroplasma, it is unlikely that the male killer infection has reached an abundance that would induce similar selection pressures in nature. In this thesis, I showed several aspects of how host parasite interactions shape organismal life history, highlighting parasites as a selective force mediating host resource allocation and dispersal. This thesis also demonstrates that consequences of parasitic manipulation can be potentially far reaching, including altering the behaviour of uninfected hosts in response. Further, I discuss a broad diversity of ways in which parasites benefit from manipulating host reproduction and shed light on promising avenues for future work.

Abstract

Half of all species are estimated to be parasites, making parasitism the most common symbiotic interaction between organisms. To avoid the detrimental effects of parasites, hosts have developed several adaptations to counteract parasitic attacks. These defences involve the development and maintenance of a functional immune system, alongside behavioural tactics to prevent initial contact with parasites (avoidance), fending off infection upon exposure (resistance), or mitigating their harmful effects post-infection (tolerance). In contrast, parasites have evolved various ways to exploit their hosts, while balancing proliferation in the current with transmission to a new host. Intriguingly, some parasites can manipulate host biology to facilitate increased transmission rates. Endosymbionts that live inside their arthropod hosts, for example, are well known to manipulate host reproduction, with potentially severe consequences for host population dynamics. In this thesis, I cover several aspects of host-parasite interactions, by considering optimal resource allocation towards immunity in a host experiencing different levels of sexual selection and parasite impact, the theoretical reasons why reproductive manipulations aid the spread of a parasitic endosymbiont and how dispersal strategies of host and parasite can influence the spread of a vertically transmitted male killing endosymbiont. Continued interactions between host and parasite will shape the functions and strength of a host’s immune defence. Immunocompetence can systematically differ within a species, where one sex produces higher levels of immunity. Ultimate explanations for this sexual dimorphism hypothesize that the sex experiencing higher levels of sexual selection, requires comparatively higher allocation of resources into the production of sexually selected traits to successfully attain fitness, thereby sacrificing immunity. Modelling a tradeoff between investments into reproduction and immunity, I show that parasite abundance and severity can significantly alter optimal immunity investment levels towards trends that can be contrary to what is predicted by the strength of sexual selection alone. While hosts are generally expected to increase investment into immunity when facing more severe or abundant parasites, I find scenarios where immunity investment can become futile, depending on parasite traits and host immune functions. Hosts should not allocate resources towards resistance when infection is unavoidable and instead invest all resources into reproduction making the most of a small lifespan, regardless of the level of sexual selection. Investments into tolerance mechanisms remain beneficial to the host even when parasites are very abundant but should be neglected in case parasites are exceedingly severe. In hosts that are capable of both, allocating investments into immunity remains optimal for host fitness. Thus, when sexes encounter different numbers or severities of parasites, the direction of sexual dimorphism is expected to shift accordingly (chapter II). How a parasite impacts its host can vary depending on host sex, especially when one sex is crucial for parasite transmission. Parasitic endosymbionts transmit almost exclusively vertically from a female host to her offspring, while male hosts represent an evolutionary dead-end to the parasite. To enhance spread through the host population, these endosymbionts evolved conceptually distinct strategies to manipulate host reproduction. I present all cases of reproductive manipulation currently known in arthropod hosts (male killing, feminization, parthenogenesis induction, sex allocation distortion and cytoplasmic incompatibility) and describe their infection dynamics in a unified modelling framework. Using the framework, I compare the ease of spread between endosymbionts using different types of reproductive manipulations and contrast the findings with the incidence of each manipulation across different host species. With the limitation that reports on reproductive manipulations could be biased, there are large discrepancies between how common each manipulation is in natural systems and the model predictions, most likely due to mechanistic constraints, with some manipulations more easily facilitated than others (chapter III). Linking dispersal and parasitic manipulation creates an intriguing mechanism of how parasitic manipulation can indirectly shape behaviour of uninfected hosts. Remaining with endosymbionts that manipulate host reproduction, I use individual based simulations to model the evolution of host dispersal during the spread of a male killing endosymbiont in a spatially structured host population in chapter IV. Since male killing endosymbionts are transmitted vertically from mother to offspring and infected male offspring die, populations can locally run out of males, unless this effect is counteracted by immigrant males. The male killer infection can spread and persist in the host population under intermediate host dispersal patterns. Uninfected males disperse comparatively more due to male-male competition during mating. When exploring a hypothetical scenario in which the male killer can additionally influence its host’s dispersal, I find that infected and uninfected individuals evolve distinct dispersal patterns, where uninfected males and females become philopatric, leading to a shift towards overall female biased dispersal. The selection for divergent dispersal patterns emerges only after parasites become highly abundant in the population. Relating these theoretical results to the natural study system that inspired the model, the African Monarch butterfly Danaus chrysippus and the male killing endosymbiont Spiroplasma, it is unlikely that the male killer infection has reached an abundance that would induce similar selection pressures in nature. In this thesis, I showed several aspects of how host parasite interactions shape organismal life history, highlighting parasites as a selective force mediating host resource allocation and dispersal. This thesis also demonstrates that consequences of parasitic manipulation can be potentially far reaching, including altering the behaviour of uninfected hosts in response. Further, I discuss a broad diversity of ways in which parasites benefit from manipulating host reproduction and shed light on promising avenues for future work.

Statistics

Downloads

0 downloads since deposited on 14 May 2024
0 downloads since 12 months

Additional indexing

Item Type:Dissertation (cumulative)
Referees:Kokko Hanna, Lindholm Krützen Anna, Shaw Allison, Martin Simon, Lüpold Stefan, Laine Anna-Liisa
Communities & Collections:07 Faculty of Science > Institute of Evolutionary Biology and Environmental Studies
UZH Dissertations
Dewey Decimal Classification:570 Life sciences; biology
590 Animals (Zoology)
Language:English
Place of Publication:Zürich
Date:14 May 2024
Deposited On:14 May 2024 10:36
Last Modified:14 May 2024 10:40
Number of Pages:150
OA Status:Closed