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A primate phylogeny scaled to reflect the rate of bacular evolution. Darker red branches indicate lower rates of evolution; blue branches indicate particularly high rates of evolution.
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The extreme morphological variability of the baculum across mammals is thought to be the result of sexual selection ( particularly, high levels of post- copulatory selection). However, the evolutionary trajectory of the mammalian baculum is little studied and evidence for the adaptive function of the baculum has so far been elusive. Here, we use Ma...
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... chain was run for 5 million iterations with a burn-in of 50 000 iterations; this was the case for all analyses aside from the variable-rates model. We were interested in inferring seven key nodes across the mammalian phylogeny, as well as the ances- tral state of baculum presence for both the primate and carnivore orders (electronic supplementary material, figure S1). Nodes were constructed using the 'add MRCA' procedure in BAYESTRAITS [24]. ...
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... multistate analysis in BAYESTRAITS [24] (n ¼ 1818) indicates that the ancestral mammal did not possess a baculum (baculum absence, mean probability ¼ 0.98). Ancestral state reconstruc- tions across six nodes (table 1; electronic supplementary material, figure S1) suggest that the baculum first evolved after non-placental and placental mammals split (baculum absence, mean probability ¼ 0.93), but before the most recent common ancestor (MRCA) of primates and carnivores evolved (baculum presence, mean probability ¼ 0.99). The ancestral pri- mate and carnivore both had a baculum (baculum presence, mean probability ¼ 1.00 and 1.00, respectively). ...
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Variation in intensity and targets of sexual selection on multiple traits has been suggested to play a major role in promoting phenotypic differentiation between populations , although the divergence in selection may depend on year, local conditions or age. In this study, we quantified sexual selection for two putative sexual signals across two Cen...
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... Different mating systems vary in the level of postcopulatory selection and associated behavioural and morphological phenotypes they generate [24]. For example, multi-male mating systems produce high levels of postcopulatory male-male competition, and are associated with large testes to body mass ratio [5,25] and elongated bacula [24]. ...
... Different mating systems vary in the level of postcopulatory selection and associated behavioural and morphological phenotypes they generate [24]. For example, multi-male mating systems produce high levels of postcopulatory male-male competition, and are associated with large testes to body mass ratio [5,25] and elongated bacula [24]. We therefore employ mating system and testes mass (controlled for body size) as proxies for postcopulatory selection, using the compilation of data in Brindle & Opie [24]. ...
... For example, multi-male mating systems produce high levels of postcopulatory male-male competition, and are associated with large testes to body mass ratio [5,25] and elongated bacula [24]. We therefore employ mating system and testes mass (controlled for body size) as proxies for postcopulatory selection, using the compilation of data in Brindle & Opie [24]. ...
Masturbation occurs throughout the animal kingdom. At first glance, however, the fitness benefits of this self-directed behaviour are unclear. Regardless, several drivers have been proposed. Non-functional hypotheses posit that masturbation is either a pathology, or a byproduct of high underlying sexual arousal, whereas functional hypotheses argue an adaptive benefit. The Postcopulatory Selection Hypothesis states that masturbation aids the chances of fertilization, while the Pathogen Avoidance Hypothesis states that masturbation helps reduce host infection by flushing pathogens from the genital tract. Here, we present comprehensive new data documenting masturbation across the primate order and use these, in conjunction with phylogenetic comparative methods, to reconstruct the evolutionary pathways and correlates of masturbation. We find that masturbation is an ancient trait within the primate order, becoming a more common aspect of the haplorrhine behavioural repertoire after the split from tarsiers. Our analyses provide support for both the Postcopulatory Selection and Pathogen Avoidance Hypotheses in male primates, suggesting that masturbation may be an adaptive trait, functioning at a macroevolutionary scale.
... The presence of multiple functions may partly reflect the baculum's multiple evolutionary origins (Schultz et al. 2016). Analysis of bacular size and form in isolation from functional considerations therefore has limitations, but the presence of informative systematic patterns through simple analyses of size and scaling indicates that such analyses nevertheless contribute meaningfully to our understanding of bacular evolution (Arnqvist 1997;Brindle and Opie 2016;Orr and Brennan 2016). ...
Growth, allometry, and characteristics of a sexually selected structure in wolverine (Gulo gulo (Linnaeus, 1758)), northern river otter (Lontra canadensis (Linnaeus, 1758)), and sea otter (Enhydra lutris (Linnaeus, 1758))
... Gómez et al. (2016) suggested that sociality was an important mediator of conspecific aggression in mammals, so we also reconstructed an additional three components of sociality: the extent of female cooperation, the presence of bisexual groups containing multiple males, and the mating system. Furthermore, mating systems and strategies are strongly linked to the degree of competition between males (Emlen and Oring 1977;Brindle and Opie 2016), with greater variation in male reproductive success leading to higher rates of aggression, sexual dimorphism, and adaptations in response to post-copulatory competition (Clutton-Brock 2016). We therefore reconstructed infanticide along with four traits associated with the intensity of intrasexual male competition: sexual dimorphism in body size and canine size (pre-copulatory competition), the presence or absence of the penis bone (baculum), and testes size (post-copulatory competition). ...
... Infanticide was reconstructed as it represents a lethal act of conspecific violence (n=183), and high rates are reported for all African apes except bonobos (Opie et al. 2013). Also reconstructed were cooperation among females (n=41), since this can mitigate male dominance over females (e.g., in bonobos); the presence of multi-male groups (n=206), which are a prerequisite for the formation of all-male alliances; and the degree of competition between males, which can influence rates of aggression and violence (Emlen and Oring 1977;Brindle and Opie 2016). A further four traits indicative of the intensity of male-male competition were reconstructed: sexual dimorphism in body size (n=213) and canine size (n=119), mating systems (n=221), baculum presence (n=300), and testes size (n=101, details of trait states, SI table S1). ...
The origins of human intergroup conflict are poorly understood despite the volume of attention the topic has received. Recent research suggests that, among mammals, violence is especially commonplace in primates, particularly social and territorial species. Here we use Bayesian phylogenetic methods to reconstruct the evolution of lethal violence across the ape lineage to understand better the roots of human lethal violence. Of the five key traits underpinning lethal violence, our reconstructions suggest that male coalitions, male dominance over females, and male-biased territorial defence were all present in the Pan-Homo last common ancestor. However, there was no support for the presence of exclusively hostile interactions with other groups or male natal residence, contrasting with extant chimpanzees. Our results suggest humans evolved from an ancestor whose lethally violent tendencies may have been tempered, compared with extant chimpanzees, by low male relatedness and coalitions between unrelated females.
... Three key theories have been suggested, including: (i) the 'vaginal friction hypothesis' (Long & Frank, 1968), where the additional rigidity of the bacula facilitates intromission, specifically in taxa presenting high levels of sexual size dimorphism (SSD) or where the act of mounting occurs before erection (Lariviere & Ferguson, 2002); (ii) the 'prolonged intromission hypothesis' (Ewer, 1973), in which the bacula enables successful sperm deposition by preventing the urethra from becoming occluded during long periods of intromission and (iii) the 'induced ovulation hypothesis' (Greenwald, 1956), whereby the additional stiffness and/or tip shape provided by the baculum stimulates the reproductive tract of the female, triggering ovulation and increasing the likelihood of fertilisation. Support for all three hypotheses has been only sporadically found across mammals (André et al., 2021;Brindle & Opie, 2016;Dixson et al., 2004). Partly this is due to the challenges and invasiveness associated with testing these hypotheses in vivo. ...
... Previous studies have used large intraspecific datasets to examine baculum characteristics, including bone weight and length (Özen, 2018), and allometry ( Both alpha shapes PC1 and ariaDNE PC1 were significantly correlated to two proxies of post-copulatory sexual selection. These results suggest that high shape complexity, as determined by both alpha shapes and ariaDNE, may be driven by increased intromission duration across the group, supporting previous comparative studies in mammals (Brassey et al., 2020;Brindle & Opie, 2016;Dixson et al., 2004). In addition to intromission duration, there has been broad support for the prediction that relative testes mass indicates intensity of sperm competition (Birkhead & Møller, 1996;, with a recent quantitative meta-analysis justifying the use of these assumptions in research (Lüpold et al., 2020). ...
... In experimental studies, baculum form has been shown to vary with post-copulatory pressures. Artificially altered levels of sexual selection led to a significant increase in bacula width (Simmons & Firman, 2013) and baculum size was significantly associated with reproductive success (Stockley et al., 2013), suggesting that intra-sexual post-copulatory sexual selection pressure may be driving bacula evolution (Brindle & Opie, 2016). ...
The penis bone, or baculum, is present in many orders of mammals, although its function is still relatively unknown, mainly due to the challenges with studying the baculum in vivo. Suggested functions include increasing vaginal friction, prolonging intromission, and inducing ovulation. Since it is difficult to study baculum function directly, functional morphology can give important insights. Shape complexity techniques, in particular, are likely to offer a useful metric of baculum morphology, especially since finding homologous landmarks on such a structure is challenging. This study focuses on measuring baculum shape complexity in the Musteloidea ‐ a large superfamily spanning a range of body sizes with well‐developed, qualitatively diverse bacula. We compared two shape complexity metrics – Alpha shapes and AriaDNE and conducted analyses over a range of six different coefficients, or bandwidths, in 32 species of Musteloidea. Overall, we found that shape complexity, especially at the baculum distal tip, is associated with intromission duration using both metrics. These complexities can include hooks, bifurcations and other additional projections. In addition, alpha shapes complexity was also associated with relative testes mass. These results suggest that post copulatory mechanisms of sexual selection are probably driving the evolution of more complex shaped bacula tips in Musteloidea and are likely to be especially involved in increasing intromission duration during copulation. This article is protected by copyright. All rights reserved.
... Implications for reproductive biology. Several studies have explored the relationship between baculum length and the reproductive biology of the living carnivorans [e.g., [8][9][10][37][38][39][40]. These relationships can thus be used to draw inferences about the reproductive biology of the Borophaginaes. ...
The baculum of mammals offers the opportunity to study the reproductive biology of extinct species given that it is a fossilizable part of the male genitalia and that its size and shape correlate with several aspects of the reproductive biology of extant mammals. Fossil bacula, however, are rare. Currently, bacula have been described from only two extinct species of canids, one from the subfamily Caninae and the other from the extinct subfamily Hesperocyoninae. Here, I describe the bacula of five extinct species of Borophaginae, each of which was found with other skeletal elements that have enabled identification to the species level. Two specimens (Aelurodon ferox and Aelurodon stirtoni) are largely complete, while the baculum from Carpocyon compressus is complete but still embedded in matrix that obscures some of its features. The bacula of Paratomarctus euthos and Desmocyon thomsoni are incomplete, but they provide useful information nonetheless. These borophagine bacula are similar to extant canines in being robust, having a urethral groove, and a simple distal end. These features suggest that the Borophaginae had long-lasting copulation and possibly spontaneous ovulation, similar to the extant canines. However, unlike the straight baculum of extant canines, borophagine bacula are ventrally curved (arched), which is also observed in the hesperocyonine baculum. The implication of this curvature for the reproductive biology of these animals remains unknown.
... A conspicuous feature of the genitalia of some mammalian species is the baculum or penis bone. The baculum has experienced repeated gains and losses throughout mammalian evolution and exhibits considerable morphological variation among species (Brindle & Opie, 2016;Schultz et al., 2016;Stockley, 2012). Genital morphology has long been used as a means of classifying closely related species (Tuxen, 1970) and has been found to correlate strongly with mating systems, whereby male genitalia are typically more diverse in polygamous than in monogamous mating systems (Arnqvist, 1998;Dixson, 2012). ...
In species with internal fertilization, copulation is characterized by the mechanical interaction of male and female genitalia. Genital interaction during copulation stimulates the neuroendocrine system, promoting the physiological changes necessary for the initiation of pregnancy. Previous studies on mice have shown that the baculum (penis bone) influences male reproductive success under a competitive fertilization scenario and that males perform less mating behaviour and ejaculate sooner under an elevated risk of sperm competition. Here we explore how mating behaviour and baculum morphology interact to influence a male's competitive fertilization success. We selected male and female house mice, Mus musculus domesticus, from families with breeding values at the extreme of baculum shape (narrow/wide) and recorded polyandrous matings to quantify mating behaviour. Our analyses revealed that competitive fertilization success was dependent on the relative baculum shape of competing males and the amount of mating behaviour that each male delivered. Our data thereby provide support for the stimulatory hypothesis for the evolution of the mammalian baculum.
... Human reproductive anatomy more closely resembles primate species that copulate less frequently (i.e., less intense sexual selection) than promiscuous species, such as chimpanzees (details in Dixson, 2009). Simplified penile morphology, including loss of spines and baculum, occurred in Homo prior to the divergence of H. sapiens and Neanderthals (Brindle & Opie, 2016;McLean et al., 2011), suggesting extended copulation duration between pairbonded, cooperatively breeding individuals (McLean et al., 2011; but see Dixson, 2009). Vaginal size coevolves with penile size in primates (Dixson, 2009), and while a coarse measure, Neanderthal pelvic anatomy suggests vaginal dimensions similar to H. sapiens; the clitoris was likely also involved in female sexual pleasure (Wragg Sykes, 2020). ...
Despite a remarkably persistent pop culture image of Neanderthals as semi-upright, hairy, cavemen wielding clubs, science provides us with a different picture. There is no doubt that the evolutionary forces that shaped Neanderthals and Homo sapiens differed, but recent evidence of interbreeding tells us that our anatomy and physiology were compatible and differences in physical appearance were not an obstacle to social interaction. Similarities in growth and development indicate that, like us, Neanderthals also gave birth to helpless young, and imply complex social lives necessary to support reproduction and protracted phases of offspring development. Of course, some uncertainty will always surround the behaviors of extinct species, but we can be sure that Neanderthals had sex and successfully reproduced for hundreds of thousands of years, and the archeological record and DNA evidence can illuminate behaviors that are invisible anatomically. In this chapter, we synthesize diverse data, theories, and models to reconsider aspects of Neanderthal sexual and reproductive behavior, and contextualize inferences within our current understanding of their physical characteristics, life-ways, and genomics.
... Regardless of the inconclusiveness of the genes that were found based on phenotype ontology methods, 3/21 outliers for dN/dS were genes previously identified in mice as candidate genes for morphological variation in the baculum (DACT1, PTPRC, and ASPM). The baculum, or penis bone, is a novel male internal genital structure in placental mammals that evolved ~145 million years ago (Brindle & Opie, 2016), with the bear macaque, having the longest primate baculum. Since that time, it has been gained or lost multiple times, including a recent loss in Homo sapiens (Carosi & Scalici, 2017;. ...
Abstract Genital divergence is thought to contribute to reproductive barriers by establishing a “lock‐and‐key" mechanism for reproductive compatibility. One such example, Macaca arctoides, the bear macaque, has compensatory changes in both male and female genital morphology as compared to close relatives. M. arctoides also has a complex evolutionary history, having extensive introgression between the fascicularis and sinica macaque species groups. Here, phylogenetic relationships were analyzed via whole‐genome sequences from five species, including M. arctoides, and two species each from the putative parental species groups. This analysis revealed ~3x more genomic regions supported placement in the sinica species group as compared to the fascicularis species group. Additionally, introgression analysis of the M. arctoides genome revealed it is a mosaic of recent polymorphisms shared with both species groups. To examine the evolution of their unique genital morphology further, the prevalence of candidate genes involved in genital morphology was compared against genome‐wide outliers in various population genetic metrics of diversity, divergence, introgression, and selection, while accounting for background variation in recombination rate. This analysis identified 67 outlier genes, including several genes that influence baculum morphology in mice, which were of interest since the bear macaque has the longest primate baculum. The mean of four of the seven population genetic metrics was statistically different in the candidate genes as compared to the rest of the genome, suggesting that genes involved in genital morphology have increased divergence and decreased diversity beyond expectations. These results highlight specific genes that may have played a role in shaping the unique genital morphology in the bear macaque.
... 7,11,14,17,18,23 The relationship between the presence of a baculum in many nonhuman primate males and the occurrence of urolithiasis is unknown. 3 Urinary obstruction results in accumulation of toxic waste products (i.e., BUN) leading to uremia. Left untreated, this can be fatal due to resulting aberrations in acid-base status and electrolyte abnormalities. ...
Obstructive and incidental urolithiasis cases were evaluated in 5 Asian colobine monkey species (n= 21 individuals) that included 12 silvery langurs (Trachypithecus cristatus), 6 spectacled langurs (Trachypithecus obscurus), 1 Javan langur (Trachypithecus auratus auratus), 1 François' langur (Trachypithecus francoisi), and 1 red-shanked douc langur (Pygathrix nemaeus) from eight zoologic institutions. All institutions that responded were Association of Zoos and Aquariums, European Association of Zoos and Aquaria, or World Association of Zoos and Aquariums accredited. Males were more commonly represented in the total number of cases (86%), and all cases of obstructive urolithiasis occurred in males. The most common clinical signs observed in obstructive cases included stranguria (58.8%), lethargy (41.2%), anorexia (29.4%), depression (17.6%), and penile manipulation (11.8%). Clinicopathologic abnormalities revealed azotemia (76.5%), anemia (35.3%), and hyperkalemia (23.5%). Eleven of the 21 cases included urinalysis results, and crystalluria was reported in all 11. Obstructive cases were more commonly managed surgically, with medical management following. Instances of individual obstruction ranged from 0 (incidental finding) to 18, with a median of 8 (mean of 4.3) recurrent obstructions. A total of 39 urolith analyses were available from 17 of 21 cases, with calcium carbonate being the most common type isolated (37 of 39, 94.9%). Calcium oxalate was observed in the remaining 5.1% of cases (2 of 39). No cases exhibited a consistent match of crystalluria and urolith type. Death or euthanasia secondary to obstructive urolithiasis occurred in 52.4% of cases. Urinary obstruction secondary to urolithiasis appears to be a relevant cause of morbidity and mortality in Asian colobine species, and further study into etiology and preventive medicine should be undertaken.
... We aimed to obtain quantitative data about shape description and variation on a challenging bone by accessing precious museum reserves and by applying a combination of non-invasive data acquiring techniques and landmark-free techniques. Although overall research on genital bones is still far from being exhausted, no quantitative study about their morphological evolution, however, has ever tried to investigate the evolution of shape in such diverse bones, but has rather focused on size only, even represented by a very simple estimate such as length [77][78][79][80][81]. One crucial reason that explains the focus on length rather than on shape may lie in the difficulties of finding, on bone surface, the homologous references (landmarks) at the interspecific level, which are essential to apply the appropriate geometric morphometrics. ...
Computed Tomography (CT), mostly used in the medical field, has also recently been involved in Cultural Heritage studies, thanks to its efficiency and total non-invasiveness. Due to the large variety of sizes and compositions typical of Cultural Heritage objects, different X-ray sources, detectors, and setups are necessary to meet the different needs of various case studies. Here, we focus on the use of micro-CT to explore the morphology and shape of a small, neglected bone found inside the clitoris of non-human primates (the baubellum), which we obtained by accessing two prestigious primatological collections of the American Museum of Natural History (New York, NY, USA) and the National Museum of Natural History (Washington, DC, USA). Overcoming methodological limits imposed by the absence of homologous landmarks, we combined the use of the non-invasive 3D micro-CT and a recently released landmark-free shape analysis (the alpha-shape technique) to objectively describe and quantify the shape complexity of scanned primate baubella. Micro-CT provided high-resolution results, overcoming constraints linked to museum policy about non-disruptive sampling and preserving samples for future research. Finally, it proved appropriate as post-mortem sampling had no impact on protected wild primate populations.
