159 1

REPRODUCTIONREVIEW

Social control of spermatogenesis and steroidogenesis in fish: a comparative approach

María Florencia Scaia1,2, Luciano Cavallino1,2 and Matías Pandolfi1,2 1Instituto de Biodiversidad y Biología Experimental y Aplicada – CONICET, Ciudad Autónoma de Buenos Aires, Argentina and 2Departamento de Biodiversidad y Biología Experimental, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Ciudad Autónoma de Buenos Aires, Argentina Correspondence should be addressed to M Pandolfi; Email:[email protected]

Abstract

Social with hierarchical dominance systems are susceptible to changes their environment. Interactions with conspecifics can greatly affect individual’s behavior and reproductive success. This review will show how social behavior modulates gonadal steroidogenesis and spermatogenesis in African and Neotropical cichlid fish with different social systems and how this modulation regulates reproductive capacity. Social behavior and aggressiveness are strongly linked to sex steroids, glucocorticoids and neuropeptides. The challenge hypothesis suggests that behavioral interactions increase androgen levels in response to social instability, but there is little evidence regarding estradiol levels. It has been recently demonstrated that in male Cichlasoma dimerus, a Neotropical cichlid fish, the challenge hypothesis could also be extended to estrogens. InC. dimerus, dominant males have higher gonadosomatic index than subordinated; the percentage of spermatocytes and spermatids is higher in subordinates, while dominants show a greater percentage of spermatozoa. In other species of African , socially suppressed subordinate males are not reproductively incompetent maintaining some activity at every level of their reproductive axis. Axis reactivation upon social ascent is similar to the initiation of puberty in mammals, as well as the reoccurrence of puberty observed in seasonally breeding animals. In conclusion, social behavior and reproductive strategies in females cichlids are still understudied, and Neotropical cichlids still constitute a group that deserves more attention, considering cichlids’ diversity in mating systems, reproductive behavior and parental care. This review highlights the importance of performing further studies and additional research in these two areas, which still remain to be addressed. Reproduction (2020) 159 R31–R43

Introduction physiology (Fernald 2012, Fernald & Maruska 2012, Maruska et al. 2013, Ramallo et al. 2015). Cichlid fish The social environment can have profound effects on constitute ideal models to study reproductive physiology the behavior and physiology of each (Galhardo and behavior because they show diverse forms of & Oliveira 2014). Besides social cues and external parental care, such as substrate guarding, delayed and factors, individual’s physiology and motivational states immediate mouthbrooding. Moreover, they also show also contribute to determine the behavioral output variation in which sex provides parental care, whether (Tudorache et al. 2013). As a consequence, the hormonal it is biparental, female-only or male-only care. As a profile of each individual modulates reproductive consequence, during last decades they have become and social behavior (e.g. aggression) which, in turn, a group of growing interest to study social control of is affected by social interactions with conspecifics. reproduction. In this regard, cichlid fish dominance However, steroid levels are usually a result rather than and social rank are usually associated with distinct sex a cause of the social position as social and reproductive steroid hormone profiles. The most studied species to displays influence hormone levels. date are the African cichlids, while Neotropical species These intertwined and usually bidirectional effects are understudied. African and Neotropical cichlids are are of particular importance in social species in which both monophyletic and sister groups (Farias et al. 2000), hierarchical dominances are established. In such cases, and results based on mitochondrial DNA suggest that social status can greatly affect an individual’s behavior there are significantly higher rates of genetic variation and physiology through interactions with its conspecifics in Neotropical than in African taxa (Farias et al. 2000). (Sapolsky 2005). Social interactions that determine a The most popular cichlid models in which social position within a hierarchical system have profound and control of reproduction has been assessed are diverse effects over animals’ reproductive behavior and African species: Astatotilapia burtoni and

© 2020 Society for Reproduction and Fertility https://doi.org/10.1530/REP -18-0650 ISSN 1470–1626 (paper) 1741–7899 (online) Online version via https://rep.bioscientifica.com Downloaded from Bioscientifica.com at 09/25/2021 10:41:27PM via free access

-18-0650 R32 M F Scaia and others

Neolamprologus pulcher, from , and Oreochromis mossambicus, inhabitant of the Limpopo and Zambezi rivers (Neat et al. 1998, Oliveira 2009). A. burtoni is a species with a lek-like social system in which dominant territorial males aggressively defend a spawning territory and actively court females, while subordinate non-territorial males present a submissive behavior, resembling and schooling with females Figure 1 (A) Dominant pair of Cichlasoma dimerus guarding the eggs (Fernald & Hirata 1977). Females of this species also and defending the spawning site from other conspecific. (B) school and feed with other females and juveniles. Schematic representation of different social status fish on the Once gravid, a female will spawn with dominant experimental aquaria. Dom, dominant (female or male); sub 1, 2 or 3, Subordinate of different ranking (female or male). Modified from males, after which she incubates the fertilized eggs in Alonso et al. (2011). her buccal cavity for several weeks, known as maternal mouthbrooding behavior. After releasing the fry, female can defend the territory and exhibit maternal care for by dominant fish Ramallo( et al. 2015). In social tanks, a short period (Fernald & Hirata 1977). Interestingly, aggressive behavior is related to body size and social even if females of this species do not present social hierarchies tend to be stable, being dominant males the hierarchies when there are males present, in all-female largest animal of the tank (Alonso et al. 2011). This way, communities they acquire dominance phenotype and if there are no new intrusions or removal of individuals, male-typical behavior such as aggressive territorial social hierarchies are maintained. However, if social defense and courtship behavior (Renn et al. 2012). context changes, an individual can transition from On the contrary, N. pulcher is a cichlid species with dominant to subordinate, and vice versa. If a dominant cooperative breeding in which subordinate members of male is removed from his original tank and is placed in the group (so-called ‘helpers’) assist the breeding pair another tank where there is already a social hierarchy, in caring of offspring, defense of the territory against this dominant will be an intruder in this new scenario, intruders and digging shelters (Taborsky & Limberger and he will become a subordinate because resident fish 1981, Balshine et al. 2001). will display aggressive behavior, leading even to death. As most of these studies were performed in African On the contrary, if the dominant male is removed from species and considering that African and Neotropical the tank (resembling a potential capture by predator cichlids are monophyletic and sister groups in which in natural environment), the highest ranked non- Neotropicals present higher genetic variation than territorial male will acquire dominant position (personal Africans, it is important to increase research on observations). In view of its highly social behavior and understudied Neotropical cichlids. Variable reproductive effortless maintenance under laboratory conditions, physiology and behavior of the cichlid family can be chanchita has emerged as a suitable biological model better understood if new studies increase knowledge to investigate the intertwined relationship between on different cichlid species from diverse habitats and hormones, social context, and behavior. with different social systems. In order to search for Cichlid fish are interesting species to understand how the characteristics of social control of reproduction in social environment can modulate molecular, cellular and Neotropical cichlids, since 2010 we have been studying behavioral outcomes that influence reproductive success. the behavior and endocrinology of Cichlasoma dimerus, Even if social control of reproduction in cichlid fish has a South American species locally known as chanchita been already reviewed (Maruska 2014), future studies (reviewed in Ramallo et al. 2014, Silva & Pandolfi can take advantage of the extreme diversity in mating 2018). This substrate breeding fish shows biparental systems, reproductive tactics, and parental care strategies care of the eggs and larvae (Meijide & Guerrero 2000) within this group. The goal of this article is to review and undergoes multiple spawning events within a single evidence on the social control of spermatogenesis and reproductive period (November–March) (Vázquez et al. gonadal steroidogenesis in fish and how this modulation 2012). C. dimerus presents a that regulates reproductive capacity. Even though our focus determines access to breeding territories among males is on cichlid fish species, we begin by introducing and females (Alonso et al. 2011, 2012, Ramallo et al. gonadal histology and regulation of spermatogenesis 2015) (Fig. 1). Considering there is only one dominant and steroidogenesis in teleost fish. Next, we review the pair per social tank, both dominant male and female relationship between sex steroids and social behavior, aggressively defend their territory and brood. If conditions focusing on the challenge hypothesis and different and social hierarchy are maintained, the same dominant cichlid species with diverse complex social structures. pair mates repeatedly. Non-territorial individuals shoal Finally we refer to how social behavior (agonistic in subordinate mixed-sex groups, perform few and encounters, dominance/subordination and parental sporadic aggressive displays toward the dominant pair, care) can modulate spermatogenesis, steroidogenesis and are subject of highly aggressive displays performed and reproductive capacity in African and Neotropical

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Figure 2 Steroidogenic pathway in teleost fishes. Gene names of supposed enzymes are denoted on each arrow. Steroids are grouped according to the number of carbon atoms in the steroid nucleus (C18, C19, C21). cyp, cytochrome P450; hsd, hydroxysteroid dehydrogenase; OH–, hydroxy–. male cichlid fish species, focusing on the case of C. aldosterone synthesis has not been identified yet (Baker dimerus. Collectively, these studies reveal a core set of 2003). Also in teleost fish, corticosterone is an endpoint evidence summarizing the relationship between social of the steroidogenic pathway, while in humans, it is an behavior and reproduction in male cichlid fish. intermediate for the biosynthesis of aldosterone. Another main difference between these groups is regarding the maturation inducing steroids 17a,20b-dihydroxt-4- Steroidogenesis in fish pregnen-3-one and 171,20b,21-trihydroxy-4-pregnen- The core pathway of steroidogenesis in teleost fish 3-one, which induce oocyte maturation in teleost fish is similar to mammals and includes the conversion and do not exist in humans (Nagahama & Yamashita from cholesterol to steroids with 21 carbon atoms 2008). Finally, the most important difference in both (C21), while pathways involving steroids with 18 steroidogenic pathways refers to androgens. Besides and 19 carbon atoms (C18 and C19) present more , in teleost fish the main ligand for androgen differences (reviewed by Tokarz et al. 2015) (Fig. 2). receptor is the 11-KT (Kime 1993). This hormone is The cytochrome p450 cholesterol side chain cleavage synthesized via 11b-hydrox-androgens, which do not enzyme (cyp11a1), 17a-hydroxylase/lyase (cyp17a) and occur in the human androgenic pathway that is focused the aromatase (cyp19a1) are the most studied genes on 51- and 31-reductions (Miller & Auchus 2011). As in the steroidogenic pathway because they constitute a consequence, while in humans the active androgens three key steps in steroidogenesis: cyp11a1 converts are testosterone and 5a-dihydrotestosterone (DHT) cholesterol to pregnenolone as the first step of the (Mooradian et al. 1987) in fish the major androgens steroidogenic pathway, cyp17a is responsible for the are testosterone and 11-KT. Despite this, DHT with conversion of C21 steroids to C19 steroids, and cyp19a1 androgenic potency has been detected in plasma of is responsible for the formation of C18 steroids and is the fathead minnow (Pimephales promelas) (Margiotta- key enzyme-regulating sexual development in teleost Casaluci & Sumpter 2011), so further research is needed fish (Rashid et al. 2007, Mills et al. 2014). Moreover, to disentangle the importance of this androgen in other 11-beta hydroxysteroid dehydrogenase type 2 (hsd11b2) teleost species. is also a key enzyme in the steroidogenic pathway since Fish and other vertebrates are also divergent in the it has two main functions: it regulates the production genes that regulate steroidogenesis. One of the major of 11-ketotestosterone (11-KT) (Lokman et al. 2002) and differences is that fish underwent genome duplication also converts the active ligand to cortisone, an (Taylor et al. 2003), and this may have resulted in inactive form unable to bind to glucocorticoid receptors mutations and silencing, neofunctionalization or (Zachayus et al. 1994, Nematollahi et al. 2009). As a coexisting genes with different regulation (Hughes consequence, this enzyme could play a key role during 1994, Glasauer & Neuhauss 2014). For example, in social situations such as social challenges, in which both some teleost species such as Nile tilapia (Oreochromis androgen and glucocorticoid concentrations are altered niloticus) two genes for steroidogenic acute regulatory and deserves to be taken into account when studying protein (StAR) have been identified (Yu et al. 2014). social hierarchies in fish (Filby et al. 2012). Besides these StAR is one of the key enzymes of steroidogenesis, key genes, which have been characterized in different since it transports cholesterol to the inner membrane teleost fish species, there are others that have received of mitochondria, which is then substrate for steroid less attention. This is the case of 17b-hydroxysteroid synthesis. However, in Nile tilapia two isoforms were dehydrogenases type 3 and type 1, which are essential for detected in different tissues, suggesting that StAR1 is the biosynthesis of 11-KT (Mindnich et al. 2005) and for involved in cortisol production in kidney, StAR2 is converting estrone to E2 (Zhou et al. 2005), respectively. involved in estrogen production in ovary and that both When comparing steroidogenesis in fish and in of them could participate in androgen production in the mammals, three main differences emerge (Miller & testes (Yu et al. 2014). This suggests that both isoforms are Auchus 2011, Tokarz et al. 2015). First of all, teleost involved in common but also in differential functions. fish seem to lack aldosterone, since this hormone has Moreover, the aromatase gene also is duplicated and not been detected and an enzyme responsible for both forms differ in their regulation (Callard et al. 2001)

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Downloaded from Bioscientifica.com at 09/25/2021 10:41:27PM via free access R34 M F Scaia and others and on their localization: while cyp19a1a is mainly more primitive taxonomic groups such as Cypriniformes, ovarian, aromatase and cyp19a1b is mainly expressed in Characiformes, and Salmoniformes (Parenti & Grier the brain (Chiang et al. 2001). As a consequence, when 2004), spermatogonia are spread throughout the germinal studying steroidogenesis and the physiological role of compartment along the testes and cysts do not migrate steroids in teleost fish, it is important to take into account during their development (Grier 1981). In general, gene duplication and to study the regulation of all in the anastomosing tubular testis the distribution of steroidogenic enzymes, regardless of their localization. spermatogonia is unrestricted, while in the lobular testis they are restricted to the distal part of the lobule, at the blind end (reviewed by de Siqueira-Silva et al. 2019). Spermatogenesis and gonadal histology in fish Despite this general pattern, there are some cases in As in all vertebrates, fish testes are organized in two which lobular testis have unrestricted spermatogonial compartments: the interstitial one, where steroidogenesis type (e.g. Synbranchus marmoratus, Cichla kelberi, takes place in Leydig cells, and the germinal tissue, Cichla intermedia, reviewed by de Siqueira-Silva et al. where spermatogenesis occurs. During these process, 2019). Moreover, intermediate forms between restricted single undifferentiated spermatogonia I passes through and unrestricted spermatogonial distribution can be numerous species-specific mitotic divisions Schulz( & found in other species, such as tilapia Oreochromis Nobrega 2011a,b), two meiosis and a morphological niloticus (Vilela et al. 2003). differentiation to originate the final male gamete, According to the habitat of each fish species, the spermatozoon. In amniotes, such as mammals, spermatogenesis can present seasonal or continuous spermatogenesis occurs in tubular testes with seminiferous activity. In testis from tropical fish species, tubules (Lombardi 1998). Sertoli cells form an epithelium spermatogenesis usually occurs throughout the year. with tight junctions that forms the ‘blood–testis barrier’ However, in several species from habitats at higher and separate the tubule into basal compartment, with latitudes, spermatogenesis can be cyclic and present mitotic spermatogonia, and adluminal compartment, in seasonal variations according to environmental cues which meiotic spermatocytes continue spermatogenesis (reviewed by Schulz et al. 2010). In this sense, in some until spermatozoa (Hess & França 2005). This way, in species spermatogenesis is active during summer, such the amniotes testes each Sertoli cell provides different as trout and carp; in others it occurs in spring, such as sea environments that allow germ cells to differentiate from bream and tench, while in others it can begin in autumn the basal to the apical compartment. Conversely, in fish and finish in spring, such as stickleback and killifish. and amphibians spermatogenesis occurs in cystic testes. The progression of spermatogenesis is regulated by a In anamniote vertebrates, each Sertoli cell encloses a delicate balance between different pituitary hormones, primary spermatogonium with its cytoplasmic processes and steroid hormones such as estrogens, androgens and forming a spermatocyst, where spermatogenesis occurs progestins (reviewed by Schulz et al. 2010). In male fish (Pudney 1998). As a consequence, each cyst contains both luteinizing hormone (LH) and follicle-stimulating a group of germ cells that share a single syncytium, hormone (FSH) regulate Leydig cell steroidogenesis, and synchronously divide and differentiate (Schulz while Sertoli cells are mainly regulated by FSH but also et al. 2010). by LH when high concentrations of this hormone can Fish with cystic testes are classified according cross-activate the FSH receptor (So et al. 2005). In turn, to the organization of the germinal epithelium, as FSH also stimulates early stages of spermatogenesis by anastomosing tubular or lobular types (reviewed by enhancing spermatogonial proliferation (Ohta et al. de Siqueira-Silva et al. 2019). In the anastomosing 2007). Furthermore, steroid hormones play a central tubular type, the germinal epithelium is branched and role controlling fish spermatogenesis. Despite the fact forms anastomoses that do not blind end in the gonadal that 17b-estradiol (E2) has been historically considered a periphery. On the other hand, Neoteleostei present the ‘female’ hormone, it is present in male fish (Amer et al. lobular testis type, in which the germinal epithelium 2001, Chaves-Pozo et al. 2007, Scaia et al. 2018b) as ends blindly at the periphery of the testes. Furthermore, well as in other vertebrates (Schlinger & Arnold 1992, two types of arrangements have been described in teleost Scaia et al. 2013, 2019). Estrogens have several effects fish testes regarding how spermatogonia are distributed on fish testes and they are a topic of growing interest. in the germinal compartment (Grier 1981; reviewed In gilthead sea bream (Sparus aurata) they inhibit the by Schulz et al. 2010, de Siqueira-Silva et al. 2019). proliferation of spermatogonia in early stages, induce In the restricted spermatogonial distribution, which apoptosis of undifferentiated spermatogonia, accelerate can be found in higher teleosts such as Atheriniformes, spermatogenesis events and induce infiltration of Cyprinodontiformes and Beloniformes (Parenti & acidophilic granulocytes, which usually occur during Grier 2004), Sertoli cells surround undifferentiated post-spawning (Chaves-Pozo et al. 2007). Moreover, in spermatogonia in the distal regions of the germinal rainbow trout (Oncorhynchus mykiss) E2 plasma levels compartment. On the other hand, in the unrestricted show an increase at the beginning of the reproductive spermatogonial distribution, which can be found in cycle when initial phases of spermatogenesis take place

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(Gomez et al. 1999). High levels of this hormone reduce The challenge hypothesis has been widely studied in the seminal fluid volume, increase the percentage of male cichlid fish with different reproductive strategies locally motile spermatozoa and could eventually lead to and parental behavior. The challenge hypothesis predicts sterility (Lahnsteiner et al. 2006). Androgens (testosterone, that androgen levels should increase as a consequence of 11-KT) play a central role in spermatogenesis. For social instability (e.g. territorial intrusion), preparing the example, they stimulate spermatogonial proliferation animal for future competitive situations (Oliveira 2004). and spermatocyte formation in guppies (Poecilia In A. burtoni, after social ascent males show an increase reticulata) and spermatocyte maturation in killifish in androgen levels, both 11-KT (Maruska & Fernald 2010) (Fostier et al. 1983). They are also especially important for and testosterone (Huffman et al. 2012). In N. pulcher, a hydration and for sperm final maturation in seminiferous cooperatively breeding cichlid fish, males displayed an tubules and efferent ducts (Rolland et al. 2013) and increase in 11-KT levels, but not testosterone levels as can induce spermiation in some species such as the amago salmon (Oncorhynchus rhodurus) (Ueda et al. 1985). However, spermiation is mainly regulated by progestins such as 17a,20b-dihydroxy-4-pregnen-3-one or 17a,20b,21-trihydroxy-4-pregnen-3-one (Ueda et al. 1985). Progestins are also central in milt production and stimulate spermatozoa motility (Baynes & Scott 1985).

Relationship between sex steroids and behavior: the challenge hypothesis As already mentioned, social behavior and dominance in cichlid fish are usually related to sex steroid hormone profiles. For example, there is a positive association between dominance and androgen and estrogen levels in males of A. burtoni (Maruska et al. 2013, O’Connell et al. 2013). In C. dimerus even though circulating androgen levels are higher in dominant males, plasma E2 levels show the opposite tendency (Ramallo et al. 2015). Moreover, higher plasma androgen levels are associated to dominant reproductive status in males of O. niloticus (Pfennig et al. 2012) and Pundamilia nyererei (Dijkstra et al. 2007). In N. pulcher androgens are also associated to dominant reproductive status in both social context Figure 3 Evidence on the challenge hypothesis in the most studied and after short periods of instability, since dominant cichlid species. (A) The challenge hypothesis suggests that male–male males present higher 11-KT but similar testosterone than aggressive interactions increase testosterone levels above the helpers (Desjardins et al. 2008, Taves et al. 2009). breeding baseline, and this stimulates aggressive behavior and Taking into account that steroid levels are usually a testosterone production even more. Most studies determine result rather than a cause of the social position, behavior testosterone and 11-ketotestosterone (11-KT), which is produced by the cyp11b/cyp11c1 and the hsd11b2. However, considering that influences hormone levels (e.g. aggression). In this testosterone can also be converted to estradiol (E2) by the aromatase regard, the challenge hypothesis suggests that male– cyp19a1a/b, recent studies also extend this hypothesis to estrogens. male aggressive interactions increase testosterone levels (B) Most studies assessing predictions of the challenge hypothesis above the breeding baseline which, in turn, stimulate refer to African cichlids and, more recently, to one Neotropical aggressive behavior and further testosterone production species. According to existing evidence, three different patterns can (Wingfield et al. 1990) (Fig. 3). This hypothesis has be described. In Astatotilapia burtoni males, 11-KT, testosterone and E2 levels increase after social ascent (Maruska & Fernald 2010, been originally proposed for song sparrows (Melospiza Huffman et al. 2012). In females of this species there is an increase in melodía) (Wingfield 1985), but it has been later extended testosterone after territorial intrusion, but there is no evidence to other bird species (Lacava et al. 2011), mammals referring 11-KT and E2 levels after this social challenge (Renn et al. (Rincon et al. 2017) and fish Desjardins( et al. 2006, 2009). In pulcher, a cooperatively breeding species, Almeida et al. 2014, Teles & Oliveira 2016, Scaia et al. when analyzing sex steroid levels as a response to territorial 2018b). Even though this hypothesis originally suggested intrusion, in males there is an increase in 11-KT levels, but not in testosterone and E , while in females there is an increase in 11-KT that androgens are expected to increase due to male– 2 and testosterone levels, but not in E2 (Desjardins et al. 2006). In the male interactions, a more recent revision discusses how Neotropical cichlid Cichlasoma dimerus recent evidence suggests androgens are also expected to fluctuate in response to that in males there is an increase in 11-KT, testosterone and E2, after season, to male–female interactions and to non-social social challenge, while in females no changes in sex steroids were environmental cues (Goymann et al. 2007). detected (Scaia et al. 2019). https://rep.bioscientifica.com Reproduction (2020) 159 R31–R43

Downloaded from Bioscientifica.com at 09/25/2021 10:41:27PM via free access R36 M F Scaia and others response to territorial intrusion (Desjardins et al. 2006). according to the parental care behavior (Wingfield This increase in 11-KT level but not in testosterone level et al. 1990), surprisingly Neotropical cichlids have been has also been demonstrated in other African cichlid understudied in this regard. In this sense, the challenge species with different breeding systems. Such is the case hypothesis has been recently tested in C. dimerus. In a of Lamprologus callipterus, in which territorial males trial involving intrasexual dyadic encounters in neutral defend a collection of shells that are used by females arenas, an increase in both testosterone and 11-KT was as shelters in which they lay their eggs and take care observed in males (Scaia et al. 2018b). Considering of the clutch and brood (Mitchell et al. 2014). It is also that this difference with the before mentioned species the case of Tropheus moorii, a monogamous species could be due to phylogenetic distance, geographical with maternal mouthbrooding (Egger et al. 2006), and or environmental constrains, or to differences in Pseudosimochromis curvifrons, species in which males reproductive and parental behavior, further studies in present a sneaking mating behavior, and the breeding other Neotropical cichlid species are necessary. strategy is maternal mouthbrooder (Kuwamura 1987). Even though aggression has been historically Using a simulated territorial intruder protocol as the analyzed in males, females also show high levels of ethological challenge trial, an increase in 11-KT, but aggressive behavior in different groups and ethological not in testosterone levels, was observed in males of contexts (Elekonich & Wingfield 2000, Langmore et al. these species after the intrusion (Hirschenhauser et al. 2002, Davis & Marler 2003). Taking into account that 2004). It is also worth mentioning that, even though this the challenge hypothesis has been initially proposed in androgen responsiveness could not be explained by the males, very few studies have assessed this hypothesis in degree of parental care, it is related to the reproductive female fish despite the fact that in some species they can behavior since it is greater among males of monogamous be as aggressive, and even more aggressive than males species and also in species with more intense pair depending on the context (Renn et al. 2009, 2012, Scaia bonding such as T. moorii (Hirschenhauser et al. 2004). et al. 2018a). In cichlid fish, female aggression varies Prediction of the challenge hypothesis has also been according to the mating and parental behavior of each tested in Oreochromis mossambicus males with different species. For example, C. dimerus is a monogamous and approaches, since social manipulation in that case was biparental species with a hierarchical social system tested in dominant males that were swapped between in which dominant females aggressively defend their groups, and also after territorial intrusion, in which a territory together with males (Pandolfi et al. 2009, male was introduced into the aquaria. Interestingly, Alonso et al. 2011, Ramallo et al. 2014). Moreover, it has only testosterone and not 11-KT increased after social been recently determined that, when exposed to dyadic manipulation in socially stable groups but not in unstable intrasexual encounters in neutral aquaria, females are ones, in which dominant males were swapped between as aggressive as males and show the same aggressive groups for five consecutive days, while neither androgen displays toward the opponent (Scaia et al. 2018a). The increased after territorial intrusion (Almeida et al. 2014). challenge hypothesis has been also assessed in females Authors discuss that this lack of increase in androgens of C. dimerus, but no increase in androgen levels were could be because of the existence of a certain androgen detected after the challenge trial (Scaia et al. 2018b). threshold, above which social challenge no longer Female aggression has been also studied in A. burtoni, induces androgen response. This way, in those cases that a polygamous and maternal mouthbrooder cichlid basal levels are below that threshold, androgen levels species in which females usually do not present social increase as a consequence of social challenge, but if hierarchies and they only adopt aggressive behavior and basal levels are above that threshold, this increase does male-typical courtship displays toward other females not take place. This way, males that have reached this in the absence of males (Renn et al. 2012, O’Connell threshold of androgen response due to social stimulation et al. 2013). They also show aggressive displays toward could become unresponsive to further social challenge. male intruders when they are caring for their brood Not much is known about endocrine regulation (Renn et al. 2009), but unfortunately female aggression of reproductive behavior and social challenge in after territorial intrusion in this species has only been Neotropical South American cichlid species compared assessed regarding maternal aggression and not in with African cichlid species. Considering cichlids show neutral aquaria. Moreover, the challenge hypothesis has diverse forms of parental care, substrate guarding is mostly also been assessed in females of this species, suggesting represented by Neotropical and Madagascar cichlids, that testosterone increases in challenged females when while mouth brooding behavior is mainly represented compared to controls (Renn et al. 2009). Regarding by African species. Moreover, even if biparental N. pulcher, which has a cooperative breeding system, behavior can be found in Neotropical and African circulating levels of 11-KT and testosterone increased in species, female care behavior is mainly represented females after simulated territorial intrusion (Desjardins in African cichlids (Goodwin et al. 1998). Taking into et al. 2006). The fact that A. burtoni and N. pulcher account these variable characteristics and considering females, but not C. dimerus, support the challenge that predictions of the challenge hypothesis can differ hypothesis could be explained considering that it has

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Downloaded from Bioscientifica.com at 09/25/2021 10:41:27PM via free access Social behavior and reproduction in cichlids R37 been suggested that predictions of this hypothesis can were examined in males after protocol of social differ according to the parental care behavior (Wingfield instability (Maruska & Fernald 2011). After removing et al. 1990). However, further studies in cichlid species the dominant male, changes in gene expression and with different reproductive and parental strategies testicular morphology were measured at different times are needed, which will disentangle the relationship during social ascension (0.5, 6, 24, 72 and 120 h). This between social challenges, reproduction and sex species showed a rapid upregulation of mRNA levels steroids in females. of FSH receptor (0.5 h) and different androgen receptor Historically androgens have been suggested as main (ARα, ARβ) and estrogen receptor (ERα, ERβa and ERβb) mediators of aggressive behavior. However, even though subtypes in the testes. LH receptor was not elevated testosterone modulates aggression, aggressive behavior until 72 h after ascent, but this increase coincided can also be observed in individuals with low circulating with elevated circulating 11-KT and early stages of androgen levels (Caldwell et al. 1984, Demas et al. spermatogenesis, suggesting a role in steroidogenesis 1999, Pinxten et al. 2003). As a consequence, androgens (Maruska et al. 2011). The spermatogenic potential of have a limited explanatory power to understand the testes, as measured by cellular composition, was regulation of aggressive behavior, and there is evidence also elevated before the overall increase in testes size suggesting the aromatization of testosterone to E2 plays during social ascent. Moreover, the presence of cysts at an important role in this sense (reviewed by Trainor all stages of spermatogenesis, coupled with lower levels et al. 2006). Estrogens have been mainly associated with of gonadotropin and steroid receptors (ARα, ARβ, ERα, female-typical behavior, but several authors suggest ERβ) in subordinate males, suggests that the BPG axis that they are key factors regulating male aggression in and spermatogenesis are maintained at a sub-threshold mammals (Ogawa et al. 1998, Toda et al. 2001), birds level in anticipation of the chance to gain a territory and (Soma et al. 2000a,b, Silverin et al. 2004) and fish (Filby become reproductively active (Fig. 4). et al. 2010, Huffman et al. 2013). In spite of this growing Differences between dominant and subordinate males evidence suggesting E2 as a key mediator of aggression, regarding testicular physiology and histology have been and despite the fact that the challenge hypothesis is also detected in the Neotropical cichlid fish C. dimerus. intrinsically related to aggressive interactions, there is Dominant males show proportionally larger testis almost no evidence exploring the potential link between than subordinated males as evidenced by their higher this hypothesis and estrogens. To our knowledge, the first gonadosomatic index (GSI) (Ramallo et al. 2015). Within study relating the challenge hypothesis to E2 is in cichlid dominant male testes, spermatozoa dominated the fish. In N. pulcher, there is no increase in E2 levels as a cellular landscape with an estimated relative abundance consequence of social instability (Desjardins et al. 2006). of 34.5%, whereas spermatocytes were the major cellular

However, there is an increase in E2 levels after social component within subordinated males’ testes (39.1%). ascent in A. burtoni males (Huffman et al. 2012). These The comparison between males of different social experiments, in which dominant males are removed status revealed that the percentages of spermatocytes creating an opportunity for reproductively suppressed and spermatids were higher in subordinated males, males to ascend in social hierarchy and status, resemble while dominant males showed a greater percentage of a common situation in the natural environment (e.g. spermatozoa (Fig. 5). As a consequence, social scenario dominant males being captured or predated). Finally, in this species not only shapes the endocrine landscape also recent evidence in C. dimerus suggests that E2 as already mentioned in section 4 (e.g. dominant males increases after a challenge trial in males, but not in females (Scaia et al. 2018b). Despite this difference between N. pulcher and C. dimerus, which could be related to different mating and parental systems or to taxonomical distance, the challenge hypothesis could be extended to estrogens and this evidence encourages further research in species with diverse social behavior.

Social control of spermatogenesis in African and Neotropical cichlid fish Even though the brain–pituitary–gonad axis (BPG) Figure 4 Spermatogenesis in testes of Astatotilapia burtoni controls reproduction in all vertebrates, vast evidence subordinate, dominant and ascending male (0.5, 6, 24, 72, 120 h after perception of social opportunity). The scheme illustrates a suggests that in different groups of fish this axis is progressive increase in absolute spermatogenic potential during socially regulated (Filby et al. 2010, Tubert et al. 2012, ascent, represented by a gradual increase in the percentage of Almeida et al. 2014, Jalabert et al. 2015). In the African advanced stages of spermatogenesis (spermatocytes, spermatids and cichlid A. burtoni, testicular morphology and physiology spermatozoa). https://rep.bioscientifica.com Reproduction (2020) 159 R31–R43

Downloaded from Bioscientifica.com at 09/25/2021 10:41:27PM via free access R38 M F Scaia and others

sort of ‘social contraceptive’ which seems to delay, rather than completely impair, spermatogenesis in subordinates (Alonso et al. 2011, Ramallo et al. 2015, 2017). Considering that spermatocytes and spermatids accumulate within subordinated males’ testis, this social constraint is particularly effective at late stages of spermatogenesis during final spermatozoa maturation (Ramallo et al. 2015). However, subordinate males still possess cysts of every spermatogenic cell type, Figure 5 Comparison of gonadosomatic index (GSI) and cellular which points for a still ongoing spermatogenesis. As a composition (spermatozoa, spermatid and spermatocyte) in testis consequence, even though dominant males were better from subordinate and dominant males of Cichlasoma dimerus. suited for immediate reproduction, subordinated males Dominant males present higher GSI than subordinate and a still hold reproductive potential. These observations predominance of spermatozoa, while spermatocytes are the constitute evidence with special ecological importance predominant cellular type in testis from subordinate males. because in case social structure becomes unstable (e.g. with higher androgens and lower estrogens), but also predation or agonistic fights) the opportunity for social affects testicular morphology and composition. ascent emerges. Similarly, evidence in N. pulcher suggest This association between GSI and social status has also that reproductive capacity of subordinates is merely been found in other cichlid species, such as O. niloticus impaired and not completely suppressed: even if they (Golan & Levavi-Sivan 2013), O. mossambicus (Oliveira have relatively smaller gonads, sperm characteristics of & Almada 1998) and Amatitlania nigrofasciata (Chee high ranked helpers were similar to those of breeders et al. 2013), since dominant males also present higher (Fitzpatrick et al. 2006). For example, small helpers GSI when compared to the physiologically suppressed have slower swimming sperm, shorter lived sperm after subordinated males. Accordingly, in C. dimerus activation and a lower percentage of motile sperm than subordinate males show higher GSI in correlation with a breeders, suggesting that their sperm would be less higher dominance index (Alonso et al. 2012). Also larger competitive. However, as helpers get larger, their sperm testes are in agreement with steroid hormone profiles, is physiologically equivalent to that of breeders. The fact as higher 11-KT levels observed in dominant males are that large helpers have sperm with similar characteristics probably associated with stimulation of Sertoli cells, to those of breeders, but that they have relatively small which in turn promote spermatogonial proliferation, gonads suggests that helpers are limited in reproductive meiosis and spermiogenesis (Miura et al. 1991). These capacity. This way, it has been suggested that rather similarities among species could imply a common than investing in gonadal development, subordinate evolutionary response to social suppression in cichlids, helpers of N. pulcher may invest in strategic somatic resulting in a reduced reproductive investment in growth, using stored energy only to rapidly enhance subordinates. Moreover, this regulation between social gonad development when breeding opportunity suppression and reproductive physiology has also been arises during social ascent (Fitzpatrick et al. 2006). detected in some mammal species. In the naked mole This is in agreement with the notion by Maruska and rats breeding males have larger reproductive tract masses Fernald (2011) suggesting that males transitioning from and higher urinary testosterone concentrations when subordinate to dominant status undergo a reactivation of compared to non-breeders, even if spermatogenesis is an already functional reproductive axis (brain–pituitary– active in both cases (Faulkes et al. 1991). Moreover, in gonads), similar to pubescent mammals. It would be primate male sifakas (Propithecus verreauxi) dominant of great interest to further analyze the dynamics in males have higher testosterone levels than subordinates, spermiogenesis reactivation and the endocrine and and this difference is even more robust during breeding molecular processes involved, as a subordinated male season (Kraus et al. 1999). Similarly, it has been of different social status can suddenly become territorial suggested that in the gray mouse lemur (Microcebus or ascend in the hierarchy. murinus), which is a prosimian primate, testosterone from subordinate males decreases after they are exposed Spermatogenesis and paternal care in to urine from dominant males (Schilling et al. 1984). Cichlasoma dimerus Considering that testosterone levels are an indirect method to estimate testicular physiology, these studies Besides social and reproductive behavior, parental care imply a suppression of reproductive physiology in can also modulate reproductive physiology in males. mammal subordinate males. Parental care represents a trade-off between the survival Interestingly, it has been suggested that the of the offspring and parents’ future reproduction (Huxley constant intimidation and attacks executed by highly 1938). Parental care is defined as any form of parental ranked fish over the lowest-ranked males exert a behavior that appears likely to increase the fitness of the

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Downloaded from Bioscientifica.com at 09/25/2021 10:41:27PM via free access Social behavior and reproduction in cichlids R39 offspring (Trivers 1974). Within the animal kingdom, mentioning that no differences were observed in E2 and fish show the greatest variety of parental care especially cortisol levels in these males among the different phases. within cichlids (Goodwin et al. 1998). Fish parental In C. dimerus, the cellular composition of testes varies behavior includes activities such as nest construction, during the reproductive and paternal care periods. Even tending, guarding and fanning of the eggs and guarding though the GSI is a common metric used to estimate of the brood from predators (Royle et al. 2012). The reproductive investment in fish, it has been suggested strategy of parental care adopted by each species is that in males it does not provide information on strongly related to the mating system. For example, cellular changes that could have important functional fish species with lek-breeding or harem systems, for consequences for sperm and steroid production (Maruska example, show a strong association with maternal et al. 1996). In the case of C. dimerus, no differences mouthbrooding, such is the case for Oreochromis sp. in the GSI were found among males in the four phases and A. burtoni (Turner & Robinson 2000). However, already described (Pm, E, HL, SL). Testes cellular there is great variability among cichlids and both composition throughout the reproductive and parental parental and reproductive strategies could also depend care period was analyzed and the proportion of each on environmental conditions. cellular type during the four phases was characterized. The endocrine system plays an important role in In this social context, males exhibiting pre-spawning the control of reproductive and parental behavior activity presented testes composed of 51.8 ± 4% mature in vertebrates (Reburn & Wynne-Edwards 1999). In spermatozoa. After spawning, E males exhibited an general, it is suggested that 11-KT and testosterone elevated mean percentage of spermatogonia B and decrease during parental care periods because of an spermatocytes (31.9 ± 5.2%; 35.9 ± 3.1, respectively) apparent incompatibility of male parental behaviors and HL males had an elevated mean percentage of with aggression (reviewed by Hirschenhauser et al. SG B (37.9 ± 3.9%), reflecting a high level of germ cell 2003). However, in N. pulcher (Desjardins et al. 2008), proliferation (Birba et al. 2015). Finally, testes from SL Lythrypnus dalli (Rodgers et al. 2006) and Parablennius males showed a more homogenous distribution of each parvicornis (Ros et al. 2004) elevated androgen levels do cell type with a preponderance of SC. A morphometric not necessarily decrease parental investment. Moreover, analysis of Leydig cells nuclear area revealed that pre- in Lepomis macrochirus males there is no androgen- spawning and E males Leydig cells averaged 1.27 times mediated trade-off between parental aggression and larger than that those of MHL and MSL and was positively nurturing behavior (Rodgers et al. 2012). Furthermore, correlated with circulating 11-KT and testosterone levels males of cichlid species with exclusive maternal care (Fig. 6). have lower plasma androgen levels than males of These data suggest that C. dimerus spermatogenesis closely related cichlid species with biparental care remains active during the parental care periods, which is (Hirschenhauser et al. 2004). in concordance with the fact that C. dimerus undergoes Regarding C. dimerus, male parental care period multiple spawning events within a single reproductive can be divided in four different phases according to period (November–March) (Vázquez et al. 2012). the developmental degree of the offspring, as has also been suggested for females of this species: pre-spawning Conclusions and future directions males (Pm, day 0), males guarding eggs (E, 1 day after fertilization (1 DAF)), males guarding hatched larvae In this review we have summarized studies suggesting (HL, 3 DAF) and males guarding swimming larvae (SL, 8 that social environment regulates spermatogenesis DAF) (Tubert et al. 2012). Males exhibiting pre-spawning and steroidogenesis in cichlid fish, thus modulating activity showed 8.4 times higher 11-KT and 5.63 times the reproductive capacity. Several evidence supports higher testosterone levels than males in the different this social regulation of reproduction: (1) agonistic stages of paternal care (Birba et al. 2015). It is worth behavior influences hormonal levels, which in

Figure 6 Spermatogenesis in testes of Cichlasoma dimerus in four different parental care phases: pre-spawning males (day 0), males guarding eggs (one DAF), males guarding hatched larvae (three DAF), and males guarding swimming larvae (eight DAF). Testes of pre-spawning males were composed of 50% of spermatozoa, whereas spermatogonia type B and spermatocytes were predominant in the subsequent parental phases. DAF, days after fertilization. https://rep.bioscientifica.com Reproduction (2020) 159 R31–R43

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