The rapid evolution of male genitalia is a nearly ubiquitous pattern across sexually reproducing organisms, likely driven by the evolutionary pressures of male-male competition, male-female interactions, and perhaps pleiotropic effects of selection. The penis of many mammalian species contains a baculum, a bone that displays astonishing morphological diversity. The evolution of baculum size and shape does not consistently correlate with any aspects of mating system, hindering our understanding of the evolutionary processes affecting it. One potential explanation for the lack of consistent comparative results is that the baculum is not actually a homologous structure. If the baculum of different groups evolved independently, then the assumption of homology inherent in comparative studies is violated. Here, we specifically test this hypothesis by modeling the presence/absence of bacula of 954 mammalian species across a well-established phylogeny and show that the baculum evolved a minimum of nine times, and was lost a minimum of ten times. Three different forms of bootstrapping show our results are robust to species sampling. Furthermore, groups with a baculum show evidence of higher rates of diversification. Our study offers an explanation for the inconsistent results in the literature, and provides insight into the evolution of this remarkable structure.
Understanding the evolutionary forces that influence sexual dimorphism is a fundamental goal in biology. Here, we focus on one particularly extreme example of sexual dimorphism. Many mammal species possess a bone in their penis called a baculum. The female equivalent of this bone is called the baubellum and occurs in the clitoris, which is developmentally homologous to the male penis. To understand the potential linkage between these two structures, we scored baculum/baubellum presence/absence across 163 species and analyzed their distribution in a phylogenetic framework. The majority of species (N = 134) shared the same state in males and females (both baculum and baubellum present or absent). However, the baubellum has experienced significantly more transitions, and more recent transitions, so that the remaining 29 species have a baculum but not a well‐developed baubellum. Even in species where both bones are present, the baubellum shows more ontogenetic variability and harbors more morphological variation than the baculum. Our study demonstrates that the baculum and baubellum are generally correlated across mammals, but that the baubellum is more evolutionarily and developmentally labile than the baculum. The accumulation of more evolutionary transitions, especially losses in the baubellum, as well as noisier developmental patterns, suggests that the baubellum may be nonfunctional, and lost over time.
The rapid divergence of male genitalia is a preeminent evolutionary pattern. This rapid divergence is especially striking in the baculum, a bone that occurs in the penis of many mammalian species. Closely related species often display diverse baculum morphology where no other morphological differences can be discerned. While this fundamental pattern of evolution has been appreciated at the level of gross morphology, nearly nothing is known about the genetic basis of size and shape divergence. Quantifying the genetic basis of baculum size and shape variation has been difficult because these structures generally lack obvious landmarks, so comparing them in three dimensions is not straightforward. Here, we develop a novel morphometric approach to quantify size and shape variation from three-dimensional micro-CT scans taken from 369 bacula, representing 75 distinct strains of the BXD family of mice. We identify two quantitative trait loci (QTL) that explain ∼50% of the variance in baculum size, and a third QTL that explains more than 20% of the variance in shape. Together, our study demonstrates that baculum morphology may diverge relatively easily, with mutations at a few loci of large effect that independently modulate size and shape. Based on a combination of bioinformatic investigations and new data on RNA expression, we prioritized these QTL to 16 candidate genes, which have hypothesized roles in bone morphogenesis and may enable future genetic manipulation of baculum morphology.
Modern morphometrics provides powerful methods to quantify size and shape variation. A basic requirement is a list of coordinates that define landmarks; however such coordinates must represent homologous structures across specimens. While many biological objects consist of easily identified landmarks to satisfy the assumption of homology, many lack such structures. One potential solution is to mathematically place semi-landmarks on an object that represent the same morphological region across specimens. Here, we illustrate a recently developed pipeline to mathematically define semi-landmarks from the mouse baculum (penis bone). Our methods should be applicable to a wide range of objects.
Modern morphometrics provides powerful methods to quantify size and shape variation. A basic requirement is a list of coordinates that define landmarks; however such coordinates must represent homologous structures across specimens. While many biological objects consist of easily identified landmarks to satisfy the assumption of homology, many lack such structures. One potential solution is to mathematically place semilandmarks on an object that represent the same morphological region across specimens. Here, we illustrate a recently developed pipeline to mathematically define semi-landmarks from the mouse baculum (penis bone). Our methods should be applicable to a wide range of objects.
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