Reproductive Immunity

Reproductive immunity involves all immune traits that assist the process of reproduction. These immune responses serve diverse functions, such as the protection and repair of reproductive tissue from mating wounds and transmitted microbes that can potentially lead to sexually transmitted infections, and can also directly bias fertilisation, such as by producing sperm antibodies or other responses that favour fertilisation by some sperm over others.

We study reproductive immunity applying an ecological immunology framework, which is founded on the basic premise that the evolution and use of the immune system are costly and thus must be traded off against other traits, such as survival and reproduction, to balance an organism’s investment into all the traits needed to promote evolutionary fitness. Localising the expression of immune agents in and surrounding attacked tissues of the host is likely to be less costly than globalised/systemic immune responses. This reduces energetic costs by keeping production of immune agents at a minimum. Also, immune agents are used when and where they are needed minimising self-harm. As with the rest of the immune response, we expect the evolution of induced and localised immune responses (relative to constitutive and global responses) to be determined by the predictability of exposure, here being wounding and/or parasite exposure and virulence. To better understand the link between reproduction and immunity as well as its maintenance we investigate selection pressures linking both biological functions and factors, such as mating rate or sperm age/health that will modulate the investment in reproductive immunity (Barribeau and Otti 2020 eLS).

Current projects 

The role of sperm adaptation and sperm plasticity in ecological speciation (DFG grant)

(Collaboration with Ondrej Balvin, Czech University of Life Sciences, Tomáš Bartonička, Masaryk University Brno and Klaus Reinhardt, Technical University Dresden funded by the DFG and GACR)

Speciation, the emergence of new species, is the ultimate source of biodiversity. Its most important step is that populations become reproductively isolated, i.e. their interbreeding is reduced or results in reduced fitness. Characters that cause reproductive isolation before mating have been intensively studied, but reproductive isolation may also occur post mating, either before or after fertilisation, called gametic isolation (prezygotic) and hybrid disadvantage. Gametic isolation is heavily understudied, and current models exclusively describe its genetic component of incompatibilities. Drawing on substantial evidence that all aspects of sperm functioning depend on genetic but environmental factors, we propose that environmental effects on sperm contribute to reproductive isolation and test it for the first time. We will investigate the relative contribution the environment has on the functioning of sperm (which, by definition, corresponds to sperm phenotypic plasticity) on reproductive isolation, compared to the (male) genetic component of sperm. We will compare the fitness outcome of population crosses in a natural system that currently undergoes speciation. We will use populations of bedbug host races that live on human or bat hosts (bat-associated lines BL and human-associated lines HL). link to paper

Ecotoxicological effects of fine particulate matter from motor combustion processes on insects (funded by the StMUV)

(Cooperative project within BayÖkotox with Heike Feldhaar, Christian Laforsch, Animal Ecology I, University of Bayreuth, Dieter Brüggemann, Engineering thermodynamics and transport processes, University Bayreuth. Bavarian State Office for the Environment (LfU) and funded by the Bavarian State Ministry of the Environment and Consumer Protection:

Many insect species, including social insects, are currently declining in abundance and diversity. Pollutants such as airborne fine particulate matter from agricultural and industrial sources are among the factors driving this decline. While these pollutants can have direct detrimental effects, they can also result in negative interactive effects when social insects are simultaneously exposed to multiple stressors. For example, sublethal effects of pollutants can increase the disease susceptibility of social insects and thereby jeopardize their survival. Here we investigate how airborne fine particulate matter interact with social insect physiology and especially the insects’ immune system. We combine ecotoxicological approaches with lab and field experiments to measure the effects of fine particles. Further, we use artificially produced fine particles from diesel engines and test their effect on bumblebee health. Bumblebees are not only ecologically important pollinators but also of tremendous economic importance in the crop pollination business. link to paper

Populationsökologie der Tiere

Host-parasite interactions in Lasius niger ant queens

(Collaboration with Simon Tragust, University of Halle, Pina Brinker, University of Groningen, Zsolt Karpati and Thomas Schmitt, University of Würzburg, Hannelore Hoch and Kristin Mahlow, Natural History Museum Berlin)

In 2015 we discovered the parasitoid fly Strongygaster globula in a local population of the black garden ant Lasius niger. Since then, we have collected queens every summer after their mating flights to investigate different aspects of this host-parasite relationship. We found some interesting behaviours in ant queens dealing with the parasitoid and currently study CHC characteristics of both antagonists and the development of the parasitoid larva inside the queen using µCT imaging and tissue clearing approaches. What once was a small side project has grown into quite an effort involving many different collaborators, and it is a fun project.

Transmission, tropism, and biological impacts of torix Rickettsia in the common bed bug

(Collaboration with Greg Hurst and Ewa Chrostek, University of Liverpool and Sophie Evison, University of Nottingham)

The torix group of Rickettsia have been recorded from a wide assemblage of invertebrates, but details of transmission and biological impacts on the host have rarely been established. The common bed bug (Cimex lectularius) is a hemipteran insect that lives as an obligatory hematophagous pest of humans and is host to a primary Wolbachia symbiont and two facultative symbionts, a BEV-like symbiont, and a torix group Rickettsia. In this study, we first note the presence of a single Rickettsia strain in multiple laboratory bed bug isolates derived from Europe and Africa. Importantly, we discovered that the Rickettsia has segregated in two laboratory strains, providing infected and uninfected isogenic lines for study. Crosses with these lines established transmission was purely maternal. Fluorescence in-situ hybridization analysis indicates Rickettsiainfection in oocytes, bacteriomes, and other somatic tissues. We found no evidence that Rickettsia infection was associated with sex ratio distortion activity, but Rickettsia infected individuals developed from the first instar to adult more slowly. The impact of Rickettsia on fecundity and fertility resulted in infected females producing fewer fertile eggs. However, we could not find any evidence for cytoplasmic incompatibility associated with Rickettsia presence. These data imply the existence of an unknown benefit to C. lectularius carrying Rickettsia that awaits further research. link to paper

Immunity to sperm

Reproductive immunity combines probably the two most important aspects of biological life: reproduction and the immune system. Reproduction incorporates highly complex processes that are mostly still unrevealed. Sexual reproduction is further complicated by the antagonistic interest of the sexes in the amount and quality of investment for reproductive output. Due to the conflicting interests, both sexes have evolved mechanisms to turn the odds of reproduction to their favour, which leads to an evolutionary arms race between the sexes. The immune system is actively involved in the processes of reproduction, mainly after insemination and during fertilisation. Post-mating processes and their relationship to immune function have just started to be described by researchers, yet without separating the effects of sperm, seminal fluid, and male effects on mating. The paragenital system of female bedbugs, into which males transfer sperm, is filled with haemocytes, suggesting that it evolved partly to reduce the immunological consequences of hypodermic sperm transfer. Different sexual selection pressures could affect the evolution of sexually transmitted diseases, adaptive suppression of immunity, sexual conflict, genetic compatibility, and cryptic female choice (CFC). CFC could drive the evolution, as immune cues potentially can provide the basis for female choice: females could directly assess male ‘quality’ by the ability of sperm to withstand, or escape, female-derived immunological attack. Sperm are non-self to a female’s immune system, and so phagocytosis may potentially act specifically on sperm. Using a phagocytosis assay, we test the selection potential of the female immune organ (mesospermalege), which was identified by Eberhard (1996) as the cryptic female choice organ. Investigating the interaction between the immune system and mating will give new insight into the processes of cryptic female choice and sperm competition within the female. Ejaculates are not only necessary for reproduction but also potentially dangerous to females. Especially, dead sperm or very old sperm should not linger around too long. Further, sperm is non-self to the female and might elicit an immune reaction, which then will kill sperm.

Outbreeding effects in an inbreeding insect

(Collaboration with Toby Fountain, University of Uppsala, Sweden)

Most populations exist with some form of spatial structure due to subdivided habitat. The common bedbug, Cimex lectularius, is rapidly re-emerging as a prominent public health and economical pest. Due to repeated founder events, frequent local extinctions due to pest control operations, and restricted dispersal, bedbugs exist in highly structured metapopulations. The number of founders has been estimated as being as low as a single mated female. Therefore, close inbreeding is likely to be a ubiquitous feature of bedbug infestations, and very high levels of differentiation have been observed between infestations. While most infestations seem to result from a single introduction, multiple introductions may be more common in buildings with a high turnover of people. Long-distance passive dispersal allows individuals from highly differentiated populations to meet and therefore introduces the possibility of heterosis and/or outbreeding depression. Whilst it is likely that bedbugs are resilient to inbreeding, as it appears that they frequently go through severe bottlenecks. What is not known is whether outbreeding can lead to a significant improvement in offspring fitness. One hypothesis may be that the increased connectivity between populations through an increase in global travel has led to a rise in outbreeding events, resulting in increased population growth and contributing to their resurgence. In this project, we investigate the effect of outbreeding of bed bugs on several different fitness correlates. We also test whether we could experimentally purge deleterious mutations with two generations of consanguineous mating. link to paper

Sexual size dimorphism in the Cimicidae

(Collaboration with Dirk J. Mikolajewski, Free University Berlin, Germany)

Sexual dimorphism is the difference between the sexes of the same species and is extremely widespread and variable in animals. It includes differences in colour, exaggerated sexually selected traits, behaviour, body structure, and size. In this project, we concentrate on sexual dimorphism (SSD), which is often female-biased in invertebrates. SSD is thought to evolve through differential selective pressures on the sexes, including fecundity selection on female size, sexual selection on male size, and genetic correlation, as well as multiple constraining factors. We are especially interested in investigating the mechanism that is central to the establishment of the size difference. Previously both development time and growth rate have been hypothesized to be important parameters in defining SSD. We investigate this by manipulating developmental time via different temperature regimes. Lower than optimal temperatures often prolong developmental times in ectothermic animals. Due to size constraints, females might be less plastic in their response to environmental stress in both these traits. Therefore, under temperature stress, SSD should be smaller at lower than optimal temperatures. Also, the growth rate should define SSD at lower than optimal temperatures rather than developmental time.

 Past projects

Sperm-microbe interactions (DFG grant)

Sara Bellinvia

Males have been proposed to protect their sperm with antimicrobial substances from sexually transmitted microbes or microbes encountered in the females. We tested this ejaculate protection hypothesis where the two basic components are examined in conjunction, 1) microbes damage sperm and 2) antimicrobial ejaculate substances prevent such microbe-induced sperm damage. For our experiments, we used the common bedbug, Cimex lectularius, which mates by traumatic insemination and possesses an antibacterial ejaculate substance. We exposed bedbug sperm to microbes either with or without antibacterial substance and measured the proportion of dead sperm. Exposure to microbes alone induced high sperm mortality, while in combination with antibacterial substance, sperm survived and a control group of sperm without antibacterial substance and microbes. We also asked ourselves if male provisioning of antibacterial substance is a nuptial gift, leading to higher offspring numbers in females. Counting eggs showed a higher egg number laid over the first few weeks and a faster decrease in egg numbers later on in the provisioned females than control groups not receiving the antibacterial substance. Sperm protection seems to be the more likely candidate for the evolution of antimicrobial substances in the seminal fluid than a nuptial gift. Although females do not seem to benefit directly from antibacterial substances, the protective effect on sperm might also reduce microbe numbers transmitted during mating. We are currently investigating to what extent microbe-induced sperm mortality translates into male fitness and, in general, how microbes affect reproductive traits of both sexes. link to paper

Cimex lectularius paramere

Cimex lectularius paramere

Future students

Please contact me if you are interested in doing a project in my group. I am happy to discuss ideas within the framework of my current projects. If you consider working with me, please have a look at this and this.