The Evolutionary Dynamics of Genetic Conflict: the Origin, Maintenance and Loss of Paternal Genome Elimination.

Reproduction across the tree of life: Why so many ways of doing it?

During sexual reproduction, two unrelated individuals cooperate to achieve a common goal: pass on their genes to the next generation. This cooperation is however not without conflict, parents can fight over who raises the kids, and partners can cheat and mate with other mates. Despite these conflicts genes of the mother and father are, at least in most animals, equally represented in the offspring. This is, however, not always the case. In my research I study a group of insects whose reproduction is incredibly variable and where evolutionary innovations appear to have reduced the importance of males. For example in the citrus mealybug (a plant parasite) and the human body lice (our own parasite), males are still needed to fertilize females, but the female can eliminate his genes from her son. This unusual type of reproduction called "Paternal Genome Elimination" (PGE) is in the female's interest as her sons will always pass on her genes, instead of those of her partner. I use these two species to study how conflict between the sexes can have lead to the evolution of this strange reproductive behaviour.

I aim to understand how males and females compete by studying the behavior of their genes within their offspring, using a range of state-of-the-art genetic techniques. In mealybugs we know that a father's genes are not simply eliminated from its sons sperm, but also prevented from being expressed. I aim to study the expression of paternal genes in males of both mealybugs and lice to understand if these genes might have the opportunity to fight against their elimination.

The way a father's genes are eliminated from his sons is still unclear, although it seems to take place in the testis while sperm is produced. I aim to study the mechanism of elimination in lice by comparing the process of sperm production in males with and without PGE.

Some of the finest minds in evolutionary biology have theorized about the evolution of PGE, yet to date, none of these theories have been tested empirically. Here I will use the human body louse, in which PGE has only recently been discovered to test these theories. I will use crosses between individuals with and without PGE to study how this trait is inherited and how it can spread though the population.

In most species with PGE it seems that the mother's genes have won and ensured that they are the ones their sons will pass on to his children. This might not always be the case though. In the final project of this proposal I will study a clade of Australian insect, closely related to mealybugs. Previous research suggests that some species have lost PGE and might have reverted back to "normal" reproduction. I will study species across this clade to see how often PGE has been lost and which factors might be responsible.

Taken together, these approaches will address the forces responsible for the evolution of an unusual reproductive system. This knowledge will help scientists understand why reproduction, a process so fundamental, is so variable across life.

I identify a number of groups of beneficiaries. The proposed project is primary research, as such the primary beneficiaries will be: (1) Academic beneficiaries (for more details see previous section). In addition, we identify a set of beneficiaries that includes both academics and possible commercial partners: (2) The biological control and parasitology community. Finally, we also identify a third set of beneficiaries: (3) The general public.

(1) Academic beneficiaries
This work will make a significant contribution to the field of biology, and will increase the prestige in which the UK scientific community is already perceived. Using an empirical and highly original approach, I will study the importance of genomic conflict, a topic that has generated a lot of interest in the community but which few labs have been able to address empirically. I therefore expect this work to generate considerable interest within the scientific community. Furthermore the proposed project uses state-of-the-art genomics techniques developed by epigenesists, to study insect reproduction in non-model organisms, showing that these techniques are transferable across fields and organisms. Finally, my work has captured the interest of a large number of international collaborators that are attracted by my unique approach. Collaborating with these researchers has introduced me to novel approaches and will allow me to attract international science funding. For example my previous collaborations with US researchers has resulted in a role of senior collaborator on two recently submitted NSF grants. Taken together these approaches, collaborations and expected results will increase my scientific breadth as well as the knowledge base of the UK scientific community.

(2) The biological control and parasitology community
Both of the insects utilized in this proposal have important implications for human wealth and health. 1) Mealybugs are among the most damaging agricultural pests to both crops and ornamentals. Some species can also act as vectors of plant pathogens. Furthermore mealybugs and other scale insects are notoriously hard to control, as they are resistant to many commonly used pesticides and are disproportionately common in invasive faunas. 2) The human body louse is a treat to human health due to its ability to act as a disease vector for typhus and trench and relapsing fever. The infection frequency of this species is on the rise, most likely due to the evolution of insecticide resistance.

Understanding the reproductive biology of pests is important to design successful pest management strategies (see pathways to impact for more details): It affects both the rate at which pests can spread, as well as the rate with which they can evolve insecticide resistance. I therefore expect my research to be of considerable interest to applied entomologist involved in pest control. As such I will regularly communicate with experts on scale insect biocontrol (e.g. Dr. Mike Copland, the director of Wyebugs a UK-based biocontrol company) and louse biology (e.g. Ian Burgess, Director of the Medical Entomology Centre).

(3) The general public.
Unusual reproductive behaviours are of considerable interest to the general public. My previous work was covered widely in the international media (including the New York Times). I aim to continue communicating my research by writing press releases for all my publications in collaboration with the University Press & Information Office. I also aim to deposit all published results into publicly available depositories and am involved in the development and maintenance of a more specific publicly available database: The Nescent funded "Tree of Sex" database (see Pathways to Impact). I will redesign my homepage to make it more accessible to a wide audience and will make the pdf's of my publications available through my website. Finally I aim to publish in open access journals whenever appropriate.