Bones of contention: The functional morphology and biomechanics of the mammalian os penis and os clitoridis

When Darwin developed his theory of natural selection, he considered that individuals with characteristics most suited to their environment were more likely to survive and reproduce. A moth that is neatly camouflaged against a tree trunk is less likely to be eaten than the moth that is garishly coloured. However, Darwin also realized that some animals have features that do not appear to help them adapt to their environment. The elaborate tail feathers of male peacocks, for example, do not seem to be particularly advantageous when navigating the jungles of India. But Darwin suggested these characteristics are due to sexual selection; individuals with traits making them more likely to win a mate (through combat or display) will go on to produce more offspring. Deer antlers, lions' manes and dancing cranes are all examples of sexual selection at work.

The genitals of animals are especially likely to experience sexual selection as they play an essential role in the delivery and reception of sperm; an individual who cannot deliver sperm effectively will produce less offspring. In several groups of mammals (including monkeys, rats, dogs, moles and bats) the males have a bone located inside their penis, known as a baculum. Humans are the only apes who do not possess a baculum. Several lab-based studies on mice have shown that males with longer or wider bacula produce more offspring. Yet exactly how the baculum improves the mating success of males remains unknown. In some species, females also possess an equivalent bone located in the clitoris, known as the baubellum. Very little is known about this structure, and its function is even more enigmatic than that of the males.

In this project, I will investigate the function of these mysterious structures in the mammal skeleton. I will test several theories about how the baculum improves the mating success of males, including, i) stiffening the penis to help with insertion, ii) straightening the urethra to ensure sperm can be delivered, and iii) stimulating females to trigger ovulation. I will test whether the possession of a baubellum in females is related to how much competition they might experience to find a mate.

I will work with the National Museum of Scotland in Edinburgh to collect carcasses of many different species of deceased mammals, including both wild and zoo animals. Genitals will be removed from carcasses and will be CT scanned at Manchester's X-ray Imaging Facility. The CT scanning process is similar to technology used in hospitals to image broken bones, and allows us to visualize 3D internal structures of genitals without cutting into (and damaging) the objects. In some instances when the specimens are not valuable however, I will remove samples of soft tissue and bone and conduct tests to determine their strength and the arrangement of fibers inside the penis.

I will also conduct a unique experiment in which the penis of a rat will be removed and then artificially inflated. The penis will be placed in a loading rig inside an X-ray machine, and will be compressed and bent during a CT scan. This will be the first time the internal structure of the penis will be visualized whilst at the same time experiencing bending. This experiment will allow us to understand more about how the baculum bone behaves, and which regions of the penis are most stressed, during sex. Based on the X-ray scans, 3D digital models of penes (both with- and without bacula) will be created, and I will run virtual computer simulations of the penis to investigate the effect the bacula has on penis stiffness. Finally, I will travel to numerous museums in the UK and abroad to gather more data on the mysterious female bone, the baubellum.

By combining aspects of traditional anatomy with high-resolution x-ray scans and detailed 3D digital models, I hope to finally resolve one of the most puzzling enigmas in mammalian biology:

What is the benefit of a penis bone?

The mechanical behaviour of an individual's genitals directly impacts upon their fitness. If reproductive structures cannot function mechanically, the individual cannot deliver or receive sperm, and cannot produce viable offspring. Across five orders of mammals, males possess a mineralized element (os penis, or baculum) within the glans of the penis, which takes on a striking array of morphologically diverse forms. The homologous bone in females (os clitoridis, or baubellum) is much more sporadic, and its occurrence and morphology are almost entirely unknown. I seek to address the previously unanswered question: Is there a biomechanical function for the os penis and os clitoridis?

I will apply high-resolution contrast-enhanced microCT to a phylogenetically diverse sample of male and female mammalian genitalia to quantify internal anatomy. I propose a novel experiment to investigate the mechanical behaviour of the baculum and associated soft tissues whilst undergoing deformation in a loading rig housed with a microCT scanner. Detailed non-linear FEA models will be generated, and results validated against strains calculated during loading. I will rigorously test functional hypotheses for the baculum including: prevention of buckling during intromission; straightening the urethra during prolonged copulus, and stimulating those females characterized by induced ovulation. The occurrence and morphology of the os clitoridis will also be documented across mammals, and potential correlations to species mating systems investigated. This unique project will reveal previously hidden aspects of genital morphology and investigate their functional significance, and will transform our understanding of mammalian reproductive biology.

There are two main beneficiaries to this project: the National Museum of Scotland and the engineering modeling and simulation community.

The National Museum of Scotland (NMS) hosts a natural history collection of international importance. Unusually amongst museums in the UK, NMS maintains a policy of active collection and curation of both native fauna and exotic zoo species under the supervision of the Principal Curator of Vertebrates Dr Andrew Kitchener (see attached Project Partner Letter of Support). Their collection of animal carcasses is unrivaled, and is an invaluable resource to researchers from a wide range of backgrounds. At present, however, lots of researchers are unaware of this potential. In my experience, many bio-engineers, chemists, material scientists and roboticists would also benefit from specimens sourced from NMS, alongside the traditional array of taxonomists, conservation biologists and palaeontologists. This project will ensure the collections of the NMS make an impact far beyond the museum by engaging with academic parties whom might not otherwise interact with zoological collections. This will result in future novel applications of natural history collections to answer important research questions.

NMS is in the top 20 of the most visited museums in the world, yet many visitors to natural history museums are unaware of the extent and diversity of the material stored away from public galleries within the collections. The NMS will benefit from this fellowship through an increased public awareness of the diversity of material available 'behind the scenes' and by shifting the perception of museum collections away from the cataloguing of 'dry dusty bones', towards active dynamic research specimens.

The engineering modeling and simulation community will benefit from this fellowship through the testing and distribution of new non-linear finite element analysis (FEA) code. Important stakeholders in this community include bioengineers, roboticists and clinicians. The community is well aware of the need to take a non-linear approach when modeling the behaviour of samples experiencing large strains and plastic deformation. Yet the extent to which currently available commercial FEA software can reliably model plastic deformation when compared to experimentally derived in vivo strains remains unclear, particularly in materials other than commonly studied bony tissues. This fellowship will, therefore, seek to provide assurance to this community as to the current benefits and limitations of this modeling approach. Additionally, a considerable proportion of the community (particularly those working for health services) do not have access to costly FEA software licenses such Abaqus or ANSYS. These groups will particularly benefit from the models and documentation created for ParaFEM as part of the proposed fellowship, as the software is entirely free and open-source.

Whilst sexual health and reproduction are undeniably topics of interest to the general public, there still remains a reluctance to openly discuss many aspects of reproductive anatomy. This is particularly the case when attempting to engage school-age children with sexual education. This fellowship will make reproductive biology a more accessible and thought-provoking topic for the general public by incorporating a wide diversity of mammals with 'weird and wonderful' genitalia, and applying novel imaging and 3D modeling techniques. By discussing the form and function of human reproductive organs in the broader evolutionary context of mammal sexual organs, my research will assist in overcoming the stigma associated with talking about sexual health.