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For Peer Review Manuscripts submitted to Integrative and Comparative Biology Neuroendocrinology of sex-role reversal Journal: Integrative and Comparative Biology Manuscript ID Draft Manuscript Type: Symposium article Date Submitted by the Forn/a Peer Review Author: Complete List of Authors: Lipshutz, Sara; Indiana University Bloomington, Biology Rosvall, Kimberly; Indiana University Bloomington, Biology sex-role reversal, female competition, neural sensitivity, testosterone, Keywords: sex steroid http://mc.manuscriptcentral.com/icbiol Page 1 of 27 Manuscripts submitted to Integrative and Comparative Biology 1 2 3 1 Neuroendocrinology of sex-role reversal 4 2 Sara E. Lipshutz1,*, Kimberly A. Rosvall1,2 5 3 6 4 1. Department of Biology, Indiana University, Bloomington, IN, 47405 7 5 2. Center for the Integrated Study of Animal Behavior, Indiana University, Bloomington, IN, 8 47405 9 6 10 7 11 8 *Corresponding author 12 9 Full address: Department of Biology, Jordan Hall Rm. 142, 1001 E. 3rd St., Indiana University, 13 10 Bloomington, IN 47405-7005, USA 14 11 Email address: [email protected] 15 12 Phone number: (812) 855-4555 16 13 Fax: (812) 855-6705 17 14 18 15 Running title: Neuroendocrinology of sex-role reversal 19 16 For Peer Review 20 17 Word count: 4,349 21 18 22 23 19 Abstract 24 25 20 Females of some species are considered sex-role reversed, meaning that they face stronger 26 27 competition for mates compared to males. While much attention has been paid to behavioral 28 21 29 30 22 and morphological patterns associated with sex-role reversal, less is known about its 31 32 23 physiological regulation. Here, we evaluate activational and organizational hypotheses relating 33 34 24 to the neuroendocrine basis of sex-role reversal. We refute the most widely tested activational 35 36 25 hypothesis for sex differences in androgen secretion; sex-role reversed females do not have 37 38 26 higher levels of androgens in circulation than males. However, we find some evidence that the 39 40 27 activational effects of androgens may be sex-specific; circulating androgen levels correlate with 41 42 28 some competitive phenotypes in sex-role reversed females. Organizational effects may explain 43 44 29 these relationships, considering that early exposure to sex steroids can shape later sensitivity to 45 46 30 hormones, often in sex-specific ways. We review evidence that sex-role reversed females have 47 48 49 31 higher tissue-specific sensitivity to androgens than males, at least in some species and tissues. 50 51 32 Moving forward, experimental and correlative studies on the ontogeny and expression of sex- 52 53 33 role reversal will help reveal the mechanisms that generate sex-specific behaviors and sex 54 55 34 roles. 56 57 58 1 59 60 http://mc.manuscriptcentral.com/icbiol Manuscripts submitted to Integrative and Comparative Biology Page 2 of 27 1 2 3 35 “Why are males masculine, females feminine and occasionally vice-versa?” 4 5 36 – GC Williams, 1975 6 7 37 8 9 10 38 An Introduction to Sex-Role Reversal 11 12 39 Why are females and males different? Biologists have been trying to answer this question 13 14 40 since Darwin first postulated that ‘instinct’ (behavior) may be shaped by natural selection (1859). 15 16 41 In his Victorian era, male animals were considered dominant and promiscuous, whereas female 17 18 42 animals were thought to be coy and subdued. In the intervening years, we have learned a lot 19 For Peer Review 20 43 about ‘sex roles’ across the animal kingdom. For many species, as Darwin and his 21 22 44 contemporaries observed, males face stronger competition for mating opportunities than females, 23 24 45 and females tend to conduct the majority of parental care (Darwin 1871; Clutton-Brock 1991; 25 26 46 Andersson 1994). Whereas territorial aggression and promiscuity were historically considered 27 28 male traits, however, behavioral ecologists now recognize that intrasexual competition and 29 47 30 31 48 multiple-mating are adaptive and widespread behaviors in females of many species (Clutton- 32 33 49 Brock 2009; Rosvall 2011; Hare and Simmons 2018). Sex-role reversal (SRR) occurs when 34 35 50 sexual selection among females is stronger than sexual selection acting among males (Vincent 36 37 51 et al. 1992; Kvarnemo and Ahnesjo 1996). SRR females are characterized by phenotypes 38 39 52 typically associated with males, including morphological traits like heavier body mass, larger 40 41 53 weaponry, and more ornamentation, as well as behavioral traits like higher territorial aggression 42 43 54 or more intense courtship rituals. These traits are thought to facilitate female-female competition 44 45 55 for mates and breeding territories (Emlen and Oring 1977; Gwynne 1991). 46 47 Classic work by Bateman (1948) and Trivers (1972) attributed the evolution of sex roles 48 56 49 50 57 to anisogamy, although this has proven challenging to reconcile with sex-role reversal. In 51 52 58 general, male gametes (sperm) are smaller and more numerous than nutrient-rich female 53 54 59 gametes (ova), and so males may be more available to mate than females, who may be 55 56 60 predisposed to caring for their offspring based on this initial asymmetry in parental investment. 57 58 2 59 60 http://mc.manuscriptcentral.com/icbiol Page 3 of 27 Manuscripts submitted to Integrative and Comparative Biology 1 2 3 61 For decades, this anisogamy argument dominated theory on the evolution of sex roles: sex 4 5 62 differences in initial parental investment drive the degree of mating competition and direction of 6 7 63 sexual selection (reviwed in Hoquet, 2020). However, anisogamy cannot explain the evolution of 8 9 10 64 SRR because SRR-females are nonetheless female; they always produce the larger gamete, 11 12 65 even when they compete more than males. Recent theoretical work indicates that additional 13 14 66 factors including multiple paternity, adult mortality, and sex ratios may generate co-evolutionary 15 16 67 feedbacks that influence the strength and sex-specificity of sexual selection (Kokko and 17 18 68 Jennions 2008; Fromhage and Jennions 2016). Despite these advances to our understanding of 19 For Peer Review 20 69 the ultimate drivers of SRR, much less is known about the proximate mechanisms that give rise 21 22 70 to SRR. 23 24 71 Sex steroids are logical candidates for the physiological regulation of SRR, because 25 26 72 these hormones are associated with many sexually dimorphic traits, especially those related to 27 28 mating and mating competition (Adkins-Regan 2005). Sex steroids act in two main ways, the 29 73 30 31 74 first of which operates early in life during a critical period when exposure to a hormone (or lack 32 33 75 thereof) can permanently organize tissue structure and function i.e. organizational effects 34 35 76 (Phoenix et al. 1959; Arnold and Breedlove 1985), which determine whether later exposure to a 36 37 77 hormone can bring about a phenotypic effect. One of the primary modes of action for 38 39 78 organizational effects is to change the anatomical distribution and/or abundance of sex steroid 40 41 79 receptors, early in the life and often lasting into adulthood (Moore et al. 1998). Activational 42 43 80 effects typically occur during adulthood, when animals change aspects of their phenotype in 44 45 81 response to changing hormone levels in circulation. For sex steroids, hormone secretion is 46 47 regulated by the hypothalamic-gonadal-pituitary (HPG) axis, when external stimuli prompt the 48 82 49 50 83 hypothalamus to secrete gonadotropin-releasing hormone (GnRH). GnRH then stimulates the 51 52 84 pituitary to release gonadotropins luteinizing hormone (LH) and follicle-stimulating hormone 53 54 85 (FSH) into the bloodstream. These gonadotropins signal to the gonads to initiate gametogenesis 55 56 86 as well as produce sex steroids including estrogen, progesterone, and testosterone, as well as 57 58 3 59 60 http://mc.manuscriptcentral.com/icbiol Manuscripts submitted to Integrative and Comparative Biology Page 4 of 27 1 2 3 87 11-ketotestosterone in fishes (Schulz et al. 2010). Many researchers have found important 4 5 88 connections between sex steroids, their cellular mechanisms of action, and the evolution of 6 7 89 sexually selected traits, linking the physiological origins of diversity in mating phenotypes across 8 9 10 90 animals (Wingfield et al. 1990; Soma 2006; Fuxjager and Schuppe 2018; Lipshutz et al. 2019; 11 12 91 Cox 2020). Critically, these mechanisms operate in both sexes (Staub and De Beer 1997), 13 14 92 providing the opportunity to investigate how variation in sex steroid signaling may contribute to 15 16 93 the origin and expression of SRR. 17 18 94 Here, we evaluate two key hypotheses on the role of sex steroids in the evolution of 19 For Peer Review 20 95 SRR. First, we examine the evidence that SRR is explained by activational effects of sex steroid 21 22 96 secretion, focusing on sex differences in levels of androgens in circulation, as well as co- 23 24 97 variation between androgens and competitive phenotypes in SRR species. Next, we assess 25 26 98 hypotheses relating to the organizational basis of SRR, asking whether androgen exposure 27 28 early in development may explain SRR behavior and morphology, and/or sex differences in 29 99 30 31 100 tissue-level sensitivity to androgens (e.g. androgen receptor abundance). We focus primarily on 32 33 101 SRR birds and fishes, which have received the most attention to date, and we draw inferences 34 35 102 from species with conventional sex roles. 36 37 103 38 39 104 H1: SRR stems from activational effects of sex steroids 40 41 105 Do females and males differ in androgen levels in circulation? 42 43 106 Two decades ago, Eens and Pinxten (2000) reviewed studies from field endocrinology to 44 45 107 evaluate the hypothesis that SRR females have male-typical physiological mechanisms, 46 47 specifically that testosterone secretion may be higher in SRR females, a reversal from the 48 108 49 50 109 conventional pattern.
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