Sexual ornaments but not weapons trade off against testes size in primates

Abstract

Males must partition their limited reproductive investments between traits that promote access to females (sexual ornaments and weapons) and traits that enhance fertilization success, such as testes and ejaculates. Recent studies show that if the most weaponized males can monopolize access to females through contest competition, thereby reducing the risk of sperm competition, they tend to invest less in sperm production. However, how males invest in sexual ornaments relative to sperm production remains less clear. If male ornaments serve as badges of status, with high-ranking males attaining near-exclusive access to females, similar to monopolizing females through combat, their expression should also covary negatively with investment in post-mating traits. In a comparative study across primates, which exhibit considerable diversification in sexual ornamentation, male weaponry and testes size, we found relative testes size to decrease with sexual ornaments but increase with canine size. These contrasting evolutionary trajectories might be driven by differential selection, functional constraints or temporal patterns of metabolic investment between the different types of sexual traits. Importantly, however, our results indicate that the theory of relative investments between weapons and testes in the context of monopolizing females can extend to male ornaments.

Evolutionary stasis of the pseudoautosomal boundary in strepsirrhine primates

“… * References are [1] Lüpold et al, 2019 , [2] Thorén et al, 2006 , [3] Gomendio et al, 2011 , [4] Harcourt et al, 1995 , [5] Lüpold, 2013 , [6] Anderson et al, 1999 , [7] Dixson and Anderson, 2004 , [8] Taylor and Schwitzer, 2011 , [9] Mittermeier et al, 2013 , [10] Soulsbury, 2010 . **or Hapalemur griseus or H. alaotrensis ***or multimale, see Soulsbury, 2010 .…”

Male morphological traits are heritable but do not predict reproductive success in a sexually-dimorphic primate

“…This finding is consistent with inter-specific analyses that have shown that species with lower levels of direct male-male competition do not exhibit strong trade-offs between investment in weaponry and investment in testis volume 10 but contrasts with intra-specific studies of other taxa, which have clearly demonstrated trade-offs between traits that are involved in pre- and post-copulatory competition 31,32,62 . This finding may also reflect different patterns of investment in canines and testes: once canines are formed, no additional energetic investment is required – in contrast, testes need to be maintained throughout adult life 12 . We would need many data points collected across the lifespan of individual males in order to test this idea.…”

“…8 ). Furthermore, there is evidence for trade-offs between traits related to pre-copulatory selection (e.g., ornaments and weaponry) and post-copulatory selection (testis volume and ejuaculates) 9–12 .…”

“…Some male traits are influenced by both male-male competition and female choice (e.g., body size in carrion flies Prochylzia xanthostma 27 , body size in pond dragonflies Libellua luctosa 28 ). Additionally, male morphology may be affected by evolutionary trade-offs between investment in traits associated with pre- and post-copulatory selection (e.g., weaponry and testes across cetacean species 29 , body mass and genital size across species of pinnipeds 30 , ornaments and testis volumes across primate species 12 , ornaments and sperm swimming speed in guppies 31 , hyoid volume and testis size in howler monkeys Alouatta spp . 32 ).…”

Measuring Pre- and Post-Copulatory Sexual Selection and Their Interaction in Socially Monogamous Species with Extra-Pair Paternity

“…Since Parker’s seminal paper 50 years ago [ 3 ], the existence of post-copulatory sexual selection has also been acknowledged, with mechanisms ranging from altering the duration of copulation, to altering the amount of parental care provided, depending on characteristics of the copulation partner [ 4 , 5 ]. More recently still, research has begun to examine the interaction between the pre-copulatory episode of sexual selection that culminates in copulation and the post-copulatory episode that culminates in fertilizing the egg [ 6 , 7 , 8 , 9 , 10 , 11 ]. If the two episodes work synergistically, they can strengthen overall selection; or if they work in opposing directions, the action of one episode may diminish the strength of selection in the other episode [ 9 , 12 , 13 ].…”