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Social Control of Spermatogenesis and Steroidogenesis in Cichlid Fish: a Comparative Approach

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Social Control of Spermatogenesis and Steroidogenesis in Cichlid Fish: a Comparative Approach 159 1 REPRODUCTIONREVIEW Social control of spermatogenesis and steroidogenesis in cichlid 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 animals 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. In C. 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 cichlids, 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 animal (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 Lake Tanganyika, 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 dominance hierarchy that regulates reproductive capacity.
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