Downloaded from http://rspb.royalsocietypublishing.org/ on April 3, 2017 Postcopulatory sexual selection influences rspb.royalsocietypublishing.org baculum evolution in primates and carnivores Matilda Brindle and Christopher Opie Research Department of Anthropology, University College London, 14 Taviton Street, London, WC1H 0BW, UK Cite this article: Brindle M, Opie C. 2016 CO, 0000-0002-3379-4703 Postcopulatory sexual selection influences baculum evolution in primates and carnivores. The extreme morphological variability of the baculum across mammals Proc. R. Soc. B 283: 20161736. is thought to be the result of sexual selection (particularly, high levels of post- copulatory selection). However, the evolutionary trajectory of the mammalian http://dx.doi.org/10.1098/rspb.2016.1736 baculum is little studied and evidence for the adaptive function of the baculum has so far been elusive. Here, we use Markov chain Monte Carlo methods implemented in a Bayesian phylogenetic framework to reconstruct baculum evolution across the mammalian class and investigate the rate of baculum Received: 5 August 2016 length evolution within the primate order. We then test the effects of testes Accepted: 4 November 2016 mass (postcopulatory sexual selection), polygamy, seasonal breeding and intromission duration on the baculum in primates and carnivores. The ances- tral mammal did not have a baculum, but both ancestral primates and carnivores did. No relationship was found between testes mass and baculum Subject Areas: length in either primates or carnivores. Intromission duration correlated with baculum presence over the course of primate evolution, and prolonged intro- evolution mission predicts significantly longer bacula in extant primates and carnivores. Both polygamous and seasonal breeding systems predict significantly longer Keywords: bacula in primates. These results suggest the baculum plays an important baculum, postcopulatory sexual selection, role in facilitating reproductive strategies in populations with high levels of prolonged intromission, primates, carnivores, postcopulatory sexual selection. Bayesian phylogenetics 1. Introduction Authors for correspondence: Matilda Brindle The morphology of male intromittent organs is argued to be subject to more rapid divergent evolution than any other form in the animal kingdom [1]. e-mail: [email protected] The baculum, or penis bone, does not buck this trend and has been described Christopher Opie as ‘the most diverse of all bones’ ([2], p. 1), varying dramatically in length, e-mail: [email protected] width and shape across the Mammalia. The baculum is not uniformly present across mammals. It was thought only to exist in eight of the mammalian orders: Afrosoricida, Carnivora, Chiroptera, Dermoptera, Erinaceomorpha, Primates, Rodentia and Soricomorpha [3,4]. How- ever, it has recently been discovered that a Lagomorph, the American pika (Ochonta princeps), also has a small baculum [5]. This discovery suggests that baculum pres- ence may be more prevalent across mammals than historically assumed. Certain orders have a mixture of baculum presence and absence across species; these are the Carnivora, Chiroptera, Primates and Rodentia. In Primates, for example, humans, tarsiers and several Platyrrhines lack a baculum. The Lagomorphia may be similarly divided. Aside from documenting the presence and absence of the baculum across the mammalian orders, the evolutionary historyof the baculum had not been studied until recently, leaving many questions unanswered. Genital (and hence bacular) morphology is suggested to be subject to sexual selection [6]. The few empirical tests conducted to date may support this hypoth- esis. Stockley et al. [7] found that baculum width in polygamous house mice (Mus Electronic supplementary material is available domesticus) was a significant predictor of male reproductive success. Simmons & online at http://dx.doi.org/10.6084/m9.fig- Firman [8] were able to manipulate baculum width experimentally by altering share.c.3583481. & 2016 The Authors. Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. Downloaded from http://rspb.royalsocietypublishing.org/ on April 3, 2017 the level of sexual selection pressure in populations of house but did not find support for the hypothesis [17]. However, 2 mice. After 27 generations, populations with artificially data to test this hypothesis were only available for 18 species, rspb.royalsocietypublishing.org enforced high levels of postcopulatory sexual selection of which only two were characterized as having short intro- pressure had significantly thicker bacula than populations in mission duration. Dixson et al. [18] argue that this sample is which monogamy was enforced and sexual selection pressure not representative enough to decisively refute the prolon- was therefore absent. These studies indicate that intra-sexual ged intromission hypothesis, and carried out their own selection, in particular postcopulatory sexual selection phylogenetically corrected analysis in a sample of 57 species pressure, may be driving bacular evolution. If this is the case, of mammal. This time, a significant correlation was found the bacula of populations under high levels of intra-sexual between the two variables. Although both studies were cor- selection pressure, such as those with polygamous (multi- rected for phylogeny, if the degree of phylogenetic male, multi-female) or seasonal mating systems, should be sub- dependency is not established before an analysis is adjusted, ject to stronger evolutionary forces. correcting for phylogeny can produce misleading or incorrect Proc. R. Soc. B Different mating systems generate variation in levels of results, as the level of relatedness between species varies postcopulatory sexual selection pressure and therefore morpho- across a phylogeny [19]. Bayesian Markov chain Monte Carlo logical variability; for example, species with high levels of (MCMC) analyses enable species’ phylogenies to be incorpor- sperm competition tend to have large testes relative to their ated into an analysis, rather than simply correcting for 283 body mass [9]. Residual testes mass is thus considered to be a phylogeny, and can thus produce more reliable results [20,21]. reliable measure of the mating system of a population and In a new study, Schultz et al. [22] used the earlier phylogenetic : 20161736 therefore the degree of sexual selection pressure [9]. Orr & methods of stochastic mapping to model the presence and Brennan [10] found that relative testes mass was a significant absence of the baculum in 954 mammalian species, and argue predictor of baculum presence across Chiroptera, Eulipotyphla, that the baculum independently evolved a minimum of nine Primates and Rodentia. However, the same study found no times in mammals. However, this sample is unlikely to reflect relationship between baculum presence or width and mating the course of evolution across the entire mammalian class, system, indicating that a third variable may be at play. Ramm particularly as baculum absence was only noted in 103 species. [11] tested for a relationship between testes mass and baculum Here, we use phylogenetic comparative methods within a length in four orders by first establishing the level of phylo- Bayesian MCMC framework [23] to examine the evolutionary genetic dependency between species and then conducting history of the baculum and investigate the hypothesis appropriately corrected regressions. A positive relationship that increased levels of intra-sexual selection affect baculum between testes mass and baculum length was noted in Rodentia evolution. We first reconstructed the evolutionary trajectory and Carnivora, but the same test found no relationship in of the baculum across the entire mammalian class and exam- Primates or Chiroptera. ined the rate of bacular evolution in the primate order. Then, The adaptive function of the baculum, under high levels we tested for a relationship between baculum length and of intra-sexual selection, is yet to be established. A potential testes mass in both primates and carnivores. We then further strategy by which a male could increase their reproductive tested for correlated evolution between baculum presence success, by outcompeting rival males, is through prolonging and intromission duration in primates, before conducting intromission and consequently delaying a female mating phylogenetic t-tests to establish whether primates and carni- with another male [12]. The prolonged intromission hypoth- vores with prolonged intromission durations have longer esis argues that the baculum helps to facilitate this prolonged bacula than those with short intromission durations. Finally, duration of intromission by supporting the penis [13]. we used the same tests to examine whether increased levels of In this context, the proximate mechanism of the baculum postcopulatory sexual selection pressure caused by (i) poly- is to act as a supportive rod, strengthening the penis and gamous mating systems and (ii) seasonal breeding patterns protecting the urethra during prolonged intromission [12]. led to an increase in baculum length in primates. Primates and A recent study on three different species of bat found that carnivores are likely to be particularly rewarding groups to the baculum formed a functional unit with the corpora caver- study,