Structure of sexual networks determines the operation PNAS PLUS of sexual selection Grant C. McDonalda,1 and Tommaso Pizzaria aEdward Grey Institute, Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom Edited by Scott V. Edwards, Harvard University, Cambridge, MA, and approved November 27, 2017 (received for review June 12, 2017) Sexual selection is a fundamental evolutionary process but remains that increasing average polyandry may strengthen sexual selection on debated, particularly in the complexity of polyandrous populations males, by allowing a subset of males to increase their reproductive where females mate with multiple males. This lack of resolution is success by mating with more females (20–23). For example, poly- partly because studies have largely ignored the structure of the andry has been suggested to drive the evolution of exaggerated sexual network, that is, the pattern of mate sharing. Here, we sexual ornaments with which males attract partners across (24, 25) quantify what we call mating assortment with network analysis to and even within species of socially monogamous birds (refs. 23 and specify explicitly the indirect as well as direct relationships between 26; see ref. 27). In contrast, other studies, often of more polyandrous partners. We first review empirical studies, showing that mating species, have suggested that increasing average polyandry may in fact assortment varies considerably in nature, due largely to basic weaken sexual selection (10, 28). These studies predict that poly- properties of the sexual network (size and density) and partly to andry should reduce variance in male mating success and limit the nonrandom patterns of mate sharing. We then use simulations to potential strength of precopulatory sexual selection because the re- show how variation in mating assortment interacts with population- level polyandry to determine the strength of sexual selection on productive benefits of mating with additional females are reduced males. Controlling for average polyandry, positive mating assort- when paternity is shared among multiple males. Thus, polyandry ment, arising when more polygynous males tend to mate with more may weaken the relationship between male mating success and re- polyandrous females, drastically decreases the intensity of pre- productive success (i.e., the Bateman gradient), and thus erode copulatory sexual selection on male mating success (Bateman precopulatory sexual selection on male mating success (4, 10, 11, 16). gradient) and the covariance between male mating success and Behavioral studies investigating the relationship between postcopulatory paternity share. Average polyandry independently precopulatory male mating success and postcopulatory paternity weakened some measures of sexual selection and crucially also share have yielded similarly inconsistent results (14). A positive impacted sexual selection indirectly by constraining mating assort- relationship between a male’s mating success and his paternity ment through the saturation of the mating network. Mating share, which would be expected to reinforce sexual selection on assortment therefore represents a key—albeit overlooked—modu- male mating success (14), has been found in several species, lator of the strength of sexual selection. Our results show that including junglefowl, Gallus gallus, guppies, Poecila reticulata, jointly considering sexual network structure and average polyandry and fruit flies, Drosophila melanogaster (10, 29–32). In other taxa, more precisely describes the strength of sexual selection. however, this relationship may be negative (33–35), indicating that precopulatory and postcopulatory episodes represent alter- Bateman gradient | mating system | opportunity for selection | SCIC | native pathways to male reproductive success, thereby creating sperm competition opportunities for alternative male mating tactics. Finally, in other species, episodes of precopulatory and postcopulatory arwin suggested that male reproductive success is typically sexual selection are largely independent (17, 36, 37). Dlimited by competitive access to fertilization opportunities and that sexual selection drives the evolution of traits conferring Significance an advantage in intrasexual competition (1). Darwin’s view of sexual selection on males was limited to competition over mating opportunities. The realization that, across many sexually repro- Sexual selection is a powerful evolutionary force, but debate ducing taxa, females often mate with multiple males so that their persists over its strength and quantification. We argue that current approaches ignore the structure of the sexual network. ejaculates overlap at the time of fertilization (polyandry) (e.g., We capture this network structure with a metric we call refs. 2 and 3), has revolutionized our understanding of sexual “mating assortment” that precisely and exhaustively captures selection (4, 5). Polyandry extends sexual selection on males the indirect as well as direct relationship between a male’s after mating (postcopulatory), via sperm competition (6) and promiscuity and that of his sexual partners. We show that cryptic female choice (7, 8), by generating variation in the pro- mating assortment is highly variable in nature and use simu- portion of a female’s eggs fertilized by her sexual partners (pa- lations to reveal that such variation plays a key—but so far ternity share). Polyandry therefore adds complexity to the unappreciated—role in determining the strength of sexual se- architecture of male reproductive success through variance in lection on males. Our results provide a clear and quantitative paternity share and covariance with precopulatory success: that method for studying sexual selection in the many mating sys- is, the number of females mated (mating success) and their fe- tems in which both polygyny and polyandry co-occur. cundity (9–14). This complexity directly affects the overall EVOLUTION strength of sexual selection and the way different selective epi- Author contributions: G.C.M. and T.P. conceived the study; G.C.M. and T.P. designed re- sodes target male traits (9, 10, 14–18). Integrating episodes of search; G.C.M. performed research; G.C.M. led the empirical review; G.C.M. analyzed precopulatory and postcopulatory sexual selection represents a data; and G.C.M. and T.P. wrote the paper. fundamental challenge for understanding the evolution of sexu- The authors declare no conflict of interest. ally selected traits and reproductive strategies (14, 18, 19). This article is a PNAS Direct Submission. A rapidly growing body of research has focused on the link be- Published under the PNAS license. tween polyandry and the operation of sexual selection on males. This 1To whom correspondence should be addressed. Email: [email protected]. effort, however, has produced contradicting results. Some studies, This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. often of species displaying low levels of polyandry, have suggested 1073/pnas.1710450115/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1710450115 PNAS | Published online December 14, 2017 | E53–E61 Downloaded by guest on September 24, 2021 A potential reason underpinning these inconsistencies is that broad range of species (Table 1 and Materials and Methods). these studies have largely focused on the average level of poly- Mating assortment in these networks vary considerably, from andry in a population or group, ignoring the details of how positive to negative (Fig. 1B and Table 1). In most networks, the polyandry varies among females and is distributed across males observed SCIC did not differ significantly from the null distri- within a group. We call this quantitative structure of variation in bution of values generated from randomizations. This indicates polyandry among females and across males “mating assortment.” that mating assortment can vary substantially even when mating The crucial point is whether highly polygynous males tend to mate between males and females occurs at random, given simple with more monogamous females (negative assortment) or with properties of the network such as network size (i.e., the number more polyandrous females (positive assortment). By describing of male and female nodes), mating density (number of mating the relationship between the polygyny of males and the polyandry pairs/total number of possible mating pairs), and the variation in of their sexual partners, mating assortment modulates the re- male and female mating success (Fig. 1B). Randomizations of lationship between male mating success (precopulatory) and the smaller networks, that is, those with fewer males and females, had intensity of sperm competition (postcopulatory), and thus can play less continuous null distributions of SCIC values as a consequence a crucial role in determining variation in male reproductive suc- of the limited number of possible permutations (SI Appendix,Fig. cess and the strength of precopulatory and postcopulatory sexual S1). Confirming previous theoretical predictions (43), our results selection (32, 38–46). Consider, for example, a population where show that for small networks both empirical estimates of SCIC males that mate with many females also tend to mate with the and their respective null distributions tended to reach more ex- most polyandrous females. This may result in those males with treme values (Fig. 2A and SI Appendix,Fig.S2). As networks greatest mating success (i.e., most