The Genetic Basis of Baculum Size and Shape Variation in Mice

Abstract

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.

Vocal divergence is concordant with genomic evidence for strong reproductive isolation in grasshopper mice (Onychomys)

“…We consider three potential mechanisms. First, baculum morphology varies greatly among species (Burt, ; Schultz et al, ) and may cause mechanical isolation (Patterson & Thaeler, ). However, O. torridus from the contact zone in NM has the most distinct baculum (Sullivan et al, ) yet successfully mated with both congeners, whereas O. arenicola and O. leucogaster have similar bacula but never reproduced in our laboratory trials.…”

“…We consider three potential mechanisms. First, baculum morphology varies greatly among species (Burt, 1960;Schultz et al, 2016) and may cause mechanical isolation (Patterson & Thaeler, 1982 (Dulac & Torello, 2003). Although the functional diversity of VRs in Onychomys is unknown, sexually dimorphic midventral sebaceous glands that secrete pheromones (Pinter, 1985) likely play a key role in sexual and, potentially, species identification.…”

A 3D journey on virtual surfaces and inner structure of ossa genitalia in Primates by means of a non-invasive imaging tool

“…https://doi.org/10.1371/journal.pone.0228131.g007 bone form variation and species reproductive and ecological correlates, in a phylogenetic perspective, might help unravelling further functional and evolutionary hypotheses. In addition, virtual data about genital bone surface could be analyzed by using either geometric morphometric techniques (for example following the same landmark and semi-landmark method applied to investigate molluscan shell shape variation by [54][55][56]) or other methods, such as the finite element analysis [57][58][59][60][61] and "alpha-shapes" [62]. In conclusion, micro-CT technique proved appropriate to discover knowledge still hidden in museum specimens or fresh 3D journey on primate ossa genitalia cadavers, preventing them not only to be stored in a closet or else get trashed after necropsy, rather allowing them to still contribute to science and live a second life.…”

Cross‐Sectional Geometry and Scaling in the Baculum of Cuban Hutias (Rodentia: Capromyidae)

“…It presents a wide diversity of size and shape across species to such an extent that it has been considered the most diverse of all bones (Patterson and Thaeler, ). It may diverge relatively easy by means of mutations at a few loci of large effect on size and shape (Schultz et al, ). It has been used widely in mammalian systematics (Martin, ; Patterson, ; Altuna and Lessa, ; Varona, ) or age determination (Friley, ; Smirnov and Tsytsulina, ).…”

“…The baculum is present in most major clades of placental mammals (Schultz et al, ) Chiroptera (except Noctilionidae, Phyllostomidae, and some species of the genus Pteropus ); a few species of Soricomorpha, Erinaceomorpha, and Afrosoricida; Carnivora (except hyenas and some viverrids); Primates (except the genera Alouatta , Ateles , Cacajao , Lagothrix , and Homo ); Dermoptera; and Rodentia. By contrast, the baculum is absent in Prototheria, Metatheria (except in the wombat), Afrotheria (except in some tenrecs), Lagomorpha (except Ochotona princeps ; see Weimann et al, ), and Xenarthra.…”