Caleb R. Ghione

The baculum, a bone in the penis of many mammal species, shows an astonishing level of morphological divergence between species. Despite hundreds of years of interest, biologists have been unable to directly test its function. The goal of the current study is to uncover molecular details that could allow selective disruption of the baculum while allowing normal sexual differentiation and skeletal development. We compare patterns of androgen receptor binding and single cell gene expression in the developing penis, forelimbs and hindlimbs of mice. We identified chondrocytes in all three tissue types, but those from the developing penis show several unique features, including a population of chondrocytes that express both Runt-related transcription factor 2 (Runx2) and Androgen receptor (Ar). By combining a Runx2-Cre allele with a floxed Ar allele in mice, we selectively knocked out androgen signaling in late chondrocytes, resulting in a range of defects in baculum morphology. Males with the most disrupted bacula were unable to copulate, and their bacula appears to be disconnected from the corpus cavernosum muscle. Our study provides insights into the diversity of molecular mechanisms leading to bone and offers the first opportunity to directly test the function of the baculum.

While spoken language is unique to humans, many features of human communication are shared with great apes, including the use of signals in multiple modalities such as vocalizations, gestures, and facial expressions. Communication signals can be unimodal (involving a single modality) or multimodal (combining multiple modalities simultaneously). Here, we examined age-related differences in bonobo ( Pan paniscus) unimodal and multimodal communication signals. We assessed all vocalizations, gestures, facial expressions, and multimodal combinations produced by captive bonobos across a variety of behavioral contexts. All occurrences of communication signals were collected via focal observations from 12 individuals ranging from 6 months to 44 years of age. All individuals produced multimodal communication signals but all bonobos, regardless of age, produced multimodal signals at lower frequencies than unimodal signals. Age had a significant effect with younger bonobos producing more multimodal signals than older individuals ( p < 0.001). The infant and juveniles produced the most multimodal signals and there was an approximately 6% increase in unimodal signals per age year increase. These findings indicate a developmental shift toward unimodal signals as bonobos age. Behavioral context was predictive of signal type usage with an increase of multimodal signals in agonistic ( p < 0.001), play ( p < 0.001), and sexual contexts ( p = 0.001). This indicates that context is important for bonobo modality with multimodal signaling occurring more in “high-risk/high-reward” contexts where proper signal comprehension is vital. This study represents an overview of multimodal communication across bonobo life stages, offering further insights into primate communication patterns and developmental trajectories.

Sexual size dimorphism is common throughout the animal kingdom, but its evolution and development remain difficult to explain given most of the genome is shared between males and females. Sex-biased regulation of genes via sex hormone signaling offers an intuitive mechanism by which males and females could develop different body sizes. One prediction of this hypothesis is that the magnitude of sexual size dimorphism scales with the number of androgen response elements or estrogen response elements, the DNA motifs to which sex hormone receptors bind. Here, we test this hypothesis using 268 mammalian species with full genome assemblies and annotations. We find that in the two smallest-bodied lineages (Chiroptera and Rodentia), sexual size dimorphism increases (male-larger) as the number of androgen response elements in a genome increases. In fact, myomorph rodents—which are especially small-bodied with high sexual size dimorphism—show an explosion of androgen receptor elements in their genomes. In contrast, the three large-bodied lineages (orders Carnivora, Cetartiodactyla, and Primates) do not show this relationship, instead following Rensch's Rule, or the observation that sexual size dimorphism increases with overall body size. One hypothesis to unify these observations is that small-bodied organisms like bats and rodents tend to reach peak reproductive fitness quickly and are more reliant on hormonal signaling to achieve sexual size dimorphism over relatively short time periods. Our study uncovers a previously unappreciated relationship between sexual size dimorphism, body size, and hormone signaling that likely varies in ways related to life history.

In mammals, a temporary endocrine gland called the corpus luteum forms on the ovary shortly after ovulation and is required for the initiation and maintenance of early pregnancy. However, the corpus luteum persists even when fertilization or pregnancy does not occur, and species-specific variation in the length of this persistence remains enigmatic. Here we perform a comparative evolutionary study across 72 species and show that corpus luteum lifespan in nonpregnant females is positively correlated with gestation length. We argue that the most likely explanation for this correlation is physiological inertia. The corpus luteum begins secreting progesterone prior to implantation, and when pregnancy does not occur it takes time for females to degrade it and prepare the next reproductive cycle. Our study suggests that this physiological inertia is stronger in species with long gestation times.

Determining how genetic polymorphisms enable certain fungi to persist in mammalian hosts can improve understanding of opportunistic fungal pathogenesis, a source of substantial human morbidity and mortality. We examined the genetic basis of fungal persistence in mice using a cross between a clinical isolate and the lab reference strain of the budding yeast Saccharomyces cerevisiae. Employing chromosomally encoded DNA barcodes, we tracked the relative abundances of 822 genotyped, haploid segregants in multiple organs over time and performed linkage mapping of their persistence in hosts. Detected loci showed a mix of general and antagonistically pleiotropic effects across organs. General loci showed similar effects across all organs, while antagonistically pleiotropic loci showed contrasting effects in the brain vs the kidneys, liver, and spleen. Persistence in an organ required both generally beneficial alleles and organ-appropriate pleiotropic alleles. This genetic architecture resulted in many segregants persisting in the brain or in nonbrain organs, but few segregants persisting in all organs. These results show complex combinations of genetic polymorphisms collectively cause and constrain fungal persistence in different parts of the mammalian body.