Variation in Plasma Steroids and Reproductive Traits in Dimorphic Males of Corkwing Wrasse (Symphodus melops L.)

doi:10.1006/hbeh.2002.1779

Hormones and Behavior

Volume 41, Issue 4, June 2002, Pages 396-404

https://doi.org/10.1006/hbeh.2002.1779 Get rights and content

Abstract

Differences in plasma steroid levels may reflect behavioral, gonadal, or morphological specializations that characterize different male reproductive phenotypes in teleost fishes. In the present study, we investigated whether differences in plasma steroid levels exist between two distinct male morphs shown in the corkwing wrasse Symphodus melops. In addition, we examined differences in male reproductive traits, including gonad mass, sperm motility, and sperm concentration, between the two male types. Possible associations between plasma steroid levels and reproductive traits were also investigated. The results indicated that males with typical male secondary sexual characters (territorial males) had higher plasma levels of 11-ketotestosterone (11kT) compared to smaller males with female secondary sexual characters (female mimics). The female mimics in turn had higher plasma levels of both testosterone (T) and 17β-estradiol. In addition, female mimics had relatively larger gonads and longer-lived sperm than territorial males. Relative gonad mass covaried significantly with the plasma levels of 11kT and T among the morphs, indicating that the relative gonad size correlates positively with the plasma level of these two steroids. However, there was no significant covariance between sperm traits and plasma steroids for the two male morphs. Hence, our results do not indicate any causal link between sperm quality and hormones.

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Reproductive and agonistic behaviours typically diverge between individuals pursuing alternative reproductive tactics (ARTs). When tactics are fixed for life, evolutionary theory predicts that the relative frequencies of alternative male genotypes are stabilized in a population by negative frequency dependence. This implies that competition is greatest between males pursuing the same tactic. The cichlid fish Lamprologus callipterus exhibits three male ARTs involving fixed and flexible tactics, and an extreme intrasexual size dimorphism determined by Mendelian inheritance. Large nest males defend territories and construct nests of empty snail shells in which females breed. In contrast, dwarf males pursuing a genetically fixed parasitic tactic enter shells surreptitiously during spawning in order to steal fertilizations. Sneaker males using another parasitic tactic, which is plastic and conditional, steal fertilizations opportunistically during spawning by quick intrusions into the nest. The variation in tactic origin and reproductive behaviour and the substantial asymmetry in body size render L. callipterus an ideal model system to study theoretical predictions regarding the types and intensity of contest behaviours among conspecific competitors pursuing ARTs. In an experiment exposing males to competitors using either the same or a different tactic, within-tactic competition was much more intense than between-tactic competition in bourgeois males, as predicted by evolutionary theory. In addition, the level of aggression displayed by bourgeois males against male intruders was apparently triggered by perceived differences in body size. In contrast to bourgeois males, parasitic males showed hardly any aggressive behaviour against other males, indicating that their contests follow the pattern of scramble competition. The conditions characterizing parasitic reproduction apparently select for rapid responsiveness when opportunities arise to fertilize eggs, whereas attacking other males in this situation seems inappropriate. Our results show that males pursuing ARTs diverge in the way they react to reproductive competition, mainly dependent on their overall resource defence strategy.
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Citation Excerpt :
No consistent pattern emerges from a comparative survey of T levels between the tactics. For example, in the peacock blenny, S. pavo [46], rock-pool blenny [61] and Atlantic salmon [70] plasma levels of T are higher in bourgeois than parasitic males, whereas the opposite is the case for the plainfin midshipman, P. notatus [7] and cockwing wrasse, Symphodus melops [73]. Contrary to the studies mentioned, we found no significant difference in plasma T concentrations between ARTs.
The proximate mechanisms that underlie the evolution of within-sex variation in mating behavior, sexual characters and reproductive investment patterns are still poorly understood. Species exhibiting alternative reproductive tactics (ARTs) are ideal model systems to examine these mechanisms. Chinook salmon (Oncorhynchus tshawytscha) exhibits two distinct ARTs: hooknoses, which are large males that establish spawning dominance hierarchies via intense male–male competition and jacks, which are smaller precocious sneaking males that steal fertilizations via sperm competition. In this study, we examine plasma testosterone (T), 11-ketotestosterone (11-KT) and maturation-inducing steroid (MIS; 17α,20β-dihydroxy-4-pregnen-3-one) profiles of spawning hooknoses and jacks. Furthermore, we examine relationships between androgens and primary (gonad mass, gonadosomatic index and sperm traits) and secondary (total mass, body size, hump depth and kype length) sexual characters. Relationships between MIS and sperm traits are also examined. We found that hooknoses and jacks did not significantly differ in terms of plasma T, 11-KT or MIS concentrations. Moreover, we found significant positive relationships between levels of both androgens within each ART. There were no significant relationships between androgens, MIS and sperm traits. T and 11-KT concentrations co-varied positively with gonad investment and kype length in jacks. In hooknoses, 11-KT concentration was positively related to total mass, hump depth and condition factor. Overall, these findings suggest that there are differential androgen effects for each of the ARTs in Chinook salmon.
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Hormones play a crucial role in mediating genetic and environmental effects into morphological and behavioral phenotypes. In systems with alternative reproductive tactics (ART) shifts between tactics are hypothesized to be under proximate hormonal control. Most studies of the underlying endocrine changes behind ART have focused on fish and amphibians rather than mammals and few have investigated the potential interaction between different endocrine axes in regulating shifts between conditional dependent tactics. Using a combination of endocrine and behavioral data from male African elephants we expand on our previously published analysis and show that the initial increase in androgens predates the behavioral shifts associated with reproductively active periods, supporting the role of androgens in activating sexually active periods in males. A strong interactive effect between androgens and glucocorticoids was found to determine the presence or absence of temporal gland secretion and urine dribbling, signals associated with the competitive reproductive tactic of musth, with elevated glucocorticoids levels suppressing the occurrence of musth signals. In addition external environmental conditions affected hormone levels. The presence of receptive females resulted in elevated androgens in dominant musth males but increased glucocorticoids in subordinate non-musth males. The presented data on hormones, behavior and reproductive tactics strongly support an underlying endocrine mechanism for mediating the translation of intrinsic as well as extrinsic local conditions into the conditional dependent reproductive tactics in male elephants via interactions between the hypothalamic-pituitary-gonadal and -adrenal axes.
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Phodopus campbelli has an extensive paternal behavior repertoire whereas the closely-related Phodopus sungorus is not paternally responsive to a displaced pup. For the first time in a naturally paternal mammal, male estradiol and progesterone were determined during two critical phases: (1) the transition from sexually naive male to paired, expectant father that occurs in the absence of stimuli from pups (sexually naive males, paired males on G8, G12, G15, or G17 of the 18-day gestation) and (2) after pup stimuli became available to the males (paired males on days L1, L3, L5, or L12 of pup development). Hormone concentrations in naive males and between G17 and L1 (as stimuli from the birth and the pups became available to males) were also compared. Paternal responsiveness was tested on L3–L5 and confirmed species differences. Hormone concentrations in naive males were similar in the two species and males of both species had estradiol concentrations as high as fertile adult females. However, in direct contrast to predictions, estradiol concentrations were stable in P. campbelli males but increased before the birth, fell across the birth, and increased over pup development in P. sungorus males. Progesterone concentrations in P. campbelli males increased from G17 to L1 whereas a decrease had been predicted. Testosterone dynamics were consistent with previous studies. Either hormonal facilitation of paternal behavior is a hyper-variable trait that has evolved differently in different species, or, more probably, peripheral hormone concentrations are inadequate to explain the role of sex steroid hormones in paternal behavior.
Reproductive Pheromones
2005, Fish Physiology
Citation Excerpt :
In many fish, relationships among male hormones, behaviour, and pheromones are further complicated by their frequent use of alternate reproductive tactics (Taborsky, 2001; see also Chapter 8). For example, in diandric species (species exhibiting more than one mature male morph), divergent phenotypic adaptations include not only different morphology and behaviour but also different concentrations of plasma androgens, 11‐ketotestosterone typically being higher in bourgeois males (males that monopolise females—sometimes known as parental males) than in parasitic males (typically smaller males that exploit investments of bourgeois males) (Borg, 1994; Taborsky, 2001; Uglem et al., 2002; see also Chapter 8). These differences raise the possibility that male morphs employ different steroidal pheromones, a situation which appears to be the case in the black goby Section 5.3.3).
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2005, Fish Physiology
Citation Excerpt :
Finally, both in the stoplight parrotfish and in the corkwing wrasse the parasitic males have significantly higher E2 levels than the bourgeois males (Cardwell and Liley, 1991; Uglem et al., 2002). Because in both species parasitic males mimic females, in particular their colouration pattern, it has been proposed that the higher levels of E2 found in parasitic males may have a feminising function (Uglem et al., 2002). This hypothesis is supported by the fact that suppression of E2 synthesis is needed for sex and colour change in protogynous hermaphroditic fish (Nakamura et al., 2003).

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Regular ArticleVariation in Plasma Steroids and Reproductive Traits in Dimorphic Males of Corkwing Wrasse (Symphodus melops L.)

Abstract

J. Theor. Biol.

Comp. Biochem. Physiol.

Horm. Behav.

Anim. Behav.

TREE.

Gen. comp. Endocrinol.

Gen. Comp. Endocr.

Horm. Behav.

Gen Comp. Endocr.

Gen. Comp. Endocrinol.

Aquaculture.

Adv. Study Behav.

TREE.

Gen. comp. Endocr.

Effects of testosterone on gonadotropins, testes and plasma 17α,20β-dihydroxy-4-pregnene-3-one levels in postbreeding mature Atlantic salmon Salmo salar, male parr

J. Exp. Zool.

Some problems related to the assessment of sperm motility in fresh-water fish

J. Exp. Zool.

Effects of gonadectomy and androgen treatments on pituitary and plasma levels of gonadotropins in mature male Atlantic salmon, Salmo salar, parr: Positive feedback control of both gonadotropins

Biol. Reprod.

Hormonal control of sex and color change in the stoplight parrotfish, Sparisoma viride (Scaridae)

Gen. Comp. Endocr.

Gonadotropin releasing hormone-analogue treatment increases sperm motility, seminal plasma pH and sperm production in yellowtail flounder Pleuronectes ferrugineus

Fish Physiol. Biochem.

Stimulation of pituitary gonadotropin by testosterone in juvenile rainbow trout (Salmo gairdneri)

Gen. Comp. Endocrinol.

The strange sex lives of British wrasse

New Scientist.

Gonochorism and sex-inversion in British Labridae (Pisces)

J. Zool., London

Characteristics of sperm of captive seabass in relation to its fertilisation potential

J. Fish Biol.

Is male germ line control creating avenues for female control

Behav. Ecol.

Effects of alternative male mating strategies on characteristics of sperm production in the Atlantic salmon (Salmo salar): Theoretical and empirical investigations

Phil. Trans. R. Soc. Lond. B

Regular Article
Variation in Plasma Steroids and Reproductive Traits in Dimorphic Males of Corkwing Wrasse (Symphodus melops L.)