Subordinate male cichlids retain reproductive competence during social suppression

Abstract

Subordinate males, which are excluded from reproduction often save energy by reducing their investment in sperm production. However, if their position in a dominance hierarchy changes suddenly they should also rapidly attain fertilization capability. Here, we asked how social suppression and ascension to dominance influences sperm quality, spermatogenesis and reproductive competence in the cichlid Astatotilapia burtoni, where reproduction is tightly coupled to social status. Dominant territorial (T) males are reproductively active while subordinate non-territorial (NT) males are suppressed, but given the opportunity, NT males will perform dominance behaviours within minutes and attain T male testes size within days. Using the thymidine analogue 5-bromo-2-deoxyuridine (BrdU) to label germ cell proliferation, we found that the spermatogenic cycle takes approximately 11 -12 days, and social status had no effect on proliferation, suggesting that spermatogenesis continues during reproductive suppression. Although sperm velocity did not differ among social states, NT males had reduced sperm motility. Remarkably, males ascending in status showed sperm motility equivalent to T males within 24 h. Males also successfully reproduced within hours of social opportunity, despite four to five weeks of suppression and reduced testis size. Our data suggest that NT males maintain reproductive potential during suppression possibly as a strategy to rapidly improve reproductive fitness upon social opportunity.

Social information changes the brain

“…However, if the nondominant male was recently dominant, despite their reduced size, the testes continue to produce sperm more slowly during the suppression period and retain viable sperm, consistent with slower cell addition generally in nondominant males (24,25). Residual sperm retention by nondominant males may allow a reproductively suppressed male to spawn with females upon social ascent without having to wait the 5-7 d for the testes to grow and the 10-11 d required for new sperm production (24). Perception of social opportunity also triggers changes in mRNA levels in the testes, on both rapid (minutes to hours; folicle-stimulating hormone receptor, androgen receptors, corticosteroid receptors) and slow (days; leuteinizing hormone receptor, aromatase, estrogen receptors) time scales (14).…”

“…However, if the nondominant male was recently dominant, despite their reduced size, the testes continue to produce sperm more slowly during the suppression period and retain viable sperm, consistent with slower cell addition generally in nondominant males (24,25). Residual sperm retention by nondominant males may allow a reproductively suppressed male to spawn with females upon social ascent without having to wait the 5-7 d for the testes to grow and the 10-11 d required for new sperm production (24).…”

Social descent with territory loss causes rapid behavioral, endocrine, and transcriptional changes in the brain

“…There is evidence in mammals that rapid adoption of submissive behaviors during hierarchical position changes can occur after watching others (Frischknecht et al, 1982), and a similar form of social learning may occur in A. burtoni (Grosenick et al, 2007). While coloration and behavioral changes that signal submission happen within minutes, physiological changes along the reproductive axis occur over days to weeks, likely as an adaptation to prolong reproductive capacity in anticipation of a future return to dominance (White et al, 2002;Maruska and Fernald, 2011b;Kustan et al, 2012). A previous study also showed that visual cues alone from a larger dominant male are sufficient to cause loss of bright coloration and submissive behaviors in a smaller dominant male (Chen and Fernald, 2011), but other sensory cues may be required for the full physiological suppression characteristic of the subordinate phenotype (Maruska and Fernald, 2010c;.…”

“…By manipulating the social environment, we can experimentally induce social transitions in either direction to test specific hypotheses about the behavioral and physiological changes that occur during natural transitions. Several studies in A. burtoni have measured changes associated with rapid social ascent from suppressed male to reproductively active territory holder (White et al, 2002;Burmeister et al, 2005;Maruska and Fernald, 2010a;Maruska and Fernald, 2011a;Maruska and Fernald, 2011b;Maruska et al, 2011;Kustan et al, 2012), but there is limited information on the effects of social descent in this species (Fox et al, 1997;Hofmann and Fernald, 2000;White et al, 2002;Parikh et al, 2006a).…”

Reproduction, olfaction and dominance behaviour in Senegalese sole (Solea senegalensis)

“…It has been reported that only a few individuals (8 -40 %) in the population contribute to offspring (Porta et al, 2006;. Social hierarchical structure is essential to achieve reproductive success in some fish species, for example in the African cichlid (Astatotilapia burtoni) only alpha males procreate while the subordinate male's reproductive system is suppressed and these males wait for a chance to take over a territory (Kustan et al, 2012). In the case of coho salmon (Onchorhynchus kisutch), two types of males are found in the population, jacks and hooknose.…”