Parasitoid species diversity has no effect on protective symbiont diversity in experimental host-parasitoid populations.

How does diversity in nature come about? One factor contributing to this diversity are species interactions; diversity on one trophic level can shape diversity on lower or higher trophic levels. For example, parasite diversity enhances host immune diversity. Insect protective symbionts mediate host resistance and are, therefore, also engaged in reciprocal selection with their host's parasites. Here, we applied experimental evolution in a well-known symbiont-aphid-parasitoid system to study whether parasitoid diversity contributes to maintaining symbiont genetic diversity. We used caged populations of black bean aphids (Aphis fabae), containing uninfected individuals and individuals infected with different strains of the bacterial endosymbiont Hamiltonella defensa, which protects aphids against parasitoids. Over multiple generations, these populations were exposed to three different species of parasitoid wasps (Aphidius colemani, Binodoxys acalephae or Lysiphlebus fabarum), simultaneous or sequential mixtures of these species or no wasps. Surprisingly, we observed little selection for H. defensa in most treatments, even when it clearly provided protection against a fatal parasitoid infection. This seemed to be caused by high induced costs of resistance: aphids surviving parasitoid attacks suffered an extreme reduction in fitness. In marked contrast to previous studies looking at the effect of different genotypes of a single parasitoid species, we found little evidence for a diversifying effect of multiple parasitoid species on symbiont diversity in hosts.

Bottom-up effect of host protective symbionts on parasitoid diversity: Limited evidence from two field experiments.

Protective symbionts can provide effective and specific protection to their hosts. This protection can differ between different symbiont strains with each strain providing protection against certain components of the parasite and pathogen community their host faces. Protective symbionts are especially well known from aphids where, among other functions, they provide protection against different parasitoid wasps. However, most of the evidence for this protection comes from laboratory experiments. Our aim was to understand how consistent protection is across different symbiont strains under natural field conditions and whether symbiont diversity enhanced the species diversity of colonizing parasitoids, as could be expected from the specificity of their protection. We used experimental colonies of the black bean aphid Aphis fabae to investigate symbiont-conferred protection under natural field conditions over two seasons. Colonies differed only in their symbiont composition, carrying either no symbionts, a single strain of the protective symbiont Hamiltonella defensa, or a mixture of three H. defensa strains. These aphid colonies were exposed to natural parasitoid communities in the field. Subsequently, we determined the parasitoids hatched from each aphid colony. The evidence for a protective effect of H. defensa was limited and inconsistent between years, and aphid colonies harbouring multiple symbiont strains did not support a more diverse parasitoid community. Instead, parasitoid diversity tended to be highest in the absence of H. defensa. Symbiont-conferred protection, although a strong and repeatable effect under laboratory conditions may not always cause the predicted bottom-up effects under natural conditions in the field.

Parasitoids as drivers of symbiont diversity in an insect host.

Immune systems have repeatedly diversified in response to parasite diversity. Many animals have outsourced part of their immune defence to defensive symbionts, which should be affected by similar evolutionary pressures as the host's own immune system. Protective symbionts provide efficient and specific protection and respond to changing selection pressure by parasites. Here we use the aphid Aphis fabae, its protective symbiont Hamiltonella defensa, and its parasitoid Lysiphlebus fabarum to test whether parasite diversity can maintain diversity in protective symbionts. We exposed aphid populations with the same initial symbiont composition to parasitoid populations that differed in their diversity. As expected, single parasitoid genotypes mostly favoured a single symbiont that was most protective against that particular parasitoid, while multiple symbionts persisted in aphids exposed to more diverse parasitoid populations, which in turn affected aphid population density and rates of parasitism. Parasite diversity may be crucial to maintaining symbiont diversity in nature.

Genomics of host-pathogen interactions: challenges and opportunities across ecological and spatiotemporal scales.

Evolutionary genomics has recently entered a new era in the study of host-pathogen interactions. A variety of novel genomic techniques has transformed the identification, detection and classification of both hosts and pathogens, allowing a greater resolution that helps decipher their underlying dynamics and provides novel insights into their environmental context. Nevertheless, many challenges to a general understanding of host-pathogen interactions remain, in particular in the synthesis and integration of concepts and findings across a variety of systems and different spatiotemporal and ecological scales. In this perspective we aim to highlight some of the commonalities and complexities across diverse studies of host-pathogen interactions, with a focus on ecological, spatiotemporal variation, and the choice of genomic methods used. We performed a quantitative review of recent literature to investigate links, patterns and potential tradeoffs between the complexity of genomic, ecological and spatiotemporal scales undertaken in individual host-pathogen studies. We found that the majority of studies used whole genome resolution to address their research objectives across a broad range of ecological scales, especially when focusing on the pathogen side of the interaction. Nevertheless, genomic studies conducted in a complex spatiotemporal context are currently rare in the literature. Because processes of host-pathogen interactions can be understood at multiple scales, from molecular-, cellular-, and physiological-scales to the levels of populations and ecosystems, we conclude that a major obstacle for synthesis across diverse host-pathogen systems is that data are collected on widely diverging scales with different degrees of resolution. This disparity not only hampers effective infrastructural organization of the data but also data granularity and accessibility. Comprehensive metadata deposited in association with genomic data in easily accessible databases will allow greater inference across systems in the future, especially when combined with open data standards and practices. The standardization and comparability of such data will facilitate early detection of emerging infectious diseases as well as studies of the impact of anthropogenic stressors, such as climate change, on disease dynamics in humans and wildlife.

Behavior out of control: Experimental evolution of resistance to host manipulation.

Many parasites alter their host's phenotype in a manner that enhances their own fitness beyond the benefits they would gain from normal exploitation. Such host manipulation is rarely consistent with the host's best interests resulting in suboptimal and often fatal behavior from the host's perspective. In this case, hosts should evolve resistance to host manipulation. The cestode Schistocephalus solidus manipulates the behavior of its first intermediate copepod host to reduce its predation susceptibility and avoid fatal premature predation before the parasite is ready for transmission to its subsequent host. Thereafter, S. solidus increases host activity to facilitate transmission. If successful, this host manipulation is necessarily fatal for the host. I selected the copepod Macrocyclops albidus, a first intermediate host of S. solidus, for resistance or susceptibility to host manipulation to investigate their evolvability. Selection on the host indeed increased host manipulation in susceptible and reduced host manipulation in resistant selection lines. Interestingly, this seemed to be at least partly due to changes in the baseline levels of the modified trait (activity) rather than actual changes in resistance or susceptibility to host manipulation. Hence, hosts seem restricted in how rapidly and efficiently they can evolve resistance to host manipulation.

Experimental evolution of parasitic host manipulation.

Host manipulation is a parasite-induced alteration of a host's phenotype that increases parasite fitness. However, if genetically encoded in the parasite, it should be under selection in the parasite. Such host manipulation has often been assumed to be energetically costly, which should restrict its evolution. Evidence of such costs, however, remains elusive. The trophically transmitted cestode Schistocephalus solidus manipulates the activity of its first intermediate copepod host to reduce its predation susceptibility before the parasite is ready for transmission. Thereafter, S. solidus increases host activity to facilitate transmission to its subsequent fish host. I selected S. solidus for or against host manipulation over three generations to investigate the evolvability of manipulation and identify potential trade-offs. Host manipulation responded to selection, confirming that this trait is heritable in the parasite and hence can present an extended phenotype. Changes in host manipulation were not restrained by any obvious costs.