From killer to carer: steroid hormones and paternal behaviour

Mammalian parental investment (i.e. care of descendant offspring) is largely biased towards maternal contributions due to the specific feeding needs of mammalian offspring; however, varying degrees of paternal investment have been reported in about 10% of all mammalian species. Within the order Carnivora, paternal contribution to rearing offspring is particularly high: an estimated 32% of all studied carnivore species exhibit direct paternal care. Despite the prominence of paternal investment in carnivores, the endocrine basis of this behaviour is not well understood. This review examines the current – highly constrained – state of knowledge about the endocrine basis of carnivore paternal investment. We attempt to link changes in androgen and glucocorticoid levels with variation in direct and indirect paternal care behaviour making specific predictions regarding the way forward. Well-studied species, such as bat-eared foxes (Otocyon megalotis), dwarf mongoose (Helogale parvula) and meerkats (Suricata suricatta), where social dynamics are relatively well understood, can act as ideal model systems through which we may further investigate the endocrine basis of paternal investment in carnivores.     

Plasma Steroid Variations in Bull Calves Repeatedly Treated with Testosterone,Nortestosterone and Oestradiol Administered Alone or in Combination

The aim of this work was to investigate the secretion of dehydroepiandrosterone (DHEA), testosterone (T), dihydrotestosterone (DHT) and oestradiol (E) as biological markers in response to illegal administration of testosterone, 19-nortestosterone (N) and oestradiol, either alone or in combination. Twenty male Friesian calves (age 13-14 months) were allotted to a control group (n = 5), and five experimental groups (n = 3) each. Each experimental animal was repeatedly injected with one of the following hormonal treatments: E, T, N, T+E and N+E. Circulating DHEA, T, DHT and E were determined by radioimmunoassay. The administration of T alone did not induce any variation in plasma DHEA, T, DHT and E, which were similar to those in the control group. In contrast, DHEA, T and DHT were on average significantly lower in the T+E and N-treated groups (p < 0.01), whereas the administration of N+E resulted in the reduction of plasma T and DHT without any modification of plasma DHEA. The administration of E alone or in combination increased circulating levels of E but did not affect androgen plasma profiles. The results indicate that plasma levels of T do not permit detection of illegal treatments because plasma androgens always remained within the physiological range. Illegal E treatment could be detected in blood samples when they were collected at least every 20 days.     

Dosage-dependent differences in the effect of aromatizable and nonaromatizable androgens on the resulting phenotype of coho salmon (Oncorhynchus kisutch)

This study was conducted to investigate whether aromatization to estrogen could be the cause for the paradoxical feminization of gonads of sexually-undifferentiated fish after treatment with androgen at either high doses or for long periods. The aromatizable androgen 17-methyltestosterone (MT) and the nonaromatizable androgen 17-methyldihydrotestosterone (MDHT) were administered to groups of newly hatched coho salmon (Oncorhynchus kisutch) in a single 2h immersion at concentrations ranging from 6.25 to 6,400µg/l. The effects of treatment were evaluated by determining the resultant proportion of males in each experimental group. The effects of steroid administration on the final mean weight, length and condition factor were also determined. An increase in all these three variables was observed in the groups treated with the higher doses of MT. Regarding the resultant sexual phenotype, the response to both androgens was similar at the majority of doses tested. However, at the highest dose, the proportion of females increased with respect to that of males for MT, but not for MDHT. Since the major difference between the two androgens tested is their capacity to be aromatized, it seems that aromatization to estrogen, rather than inhibition of the biosynthesis of endogenous androgen, may explain the paradoxical feminization encountered.     

Androgen metabolism in the skin of the rainbow trout (Oncorhynchus mykiss)

Pieces of skin of male and female rainbow trout (Oncorhynchus mykiss) were incubated with testosterone and 11-ketotestosterone as substrates. In immature fish the conversion rate was low. In non-spawning adult males 11-ketotestosterone was reduced to 5α-11KDHT (up to 5.2%). In the fish in spawning condition the 5α-reduction rate was only about 1 to 2%. In the same specimens incubated with testosterone a high 11β-hydroxylase activity (23.8-25% in the male and 13% in the female skin) was found. Similar sex specific differences were observed for the occurence of 5α-reduced metabolites (about 20% in the male and 13% in the female tissue).

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Résumé Des fragments de peau de truites arc en ciel (Oncorhynchus mykiss, males ou femelles, ont été incubés avec de la testostérone ou de la 11-cétotestostérone, utilisées comme substrats. Chez les poissons immatures, les taux de conversion restent faibles. Chez les males adultes ne donnant pas de sperme, la 11-cétotestostérone est réduite en 5α-androstane-17β-ol-3,11-dione (jusqu'à 5.2%). Chezles poissons en conditions de fraie, le taux de 5α-réduction est seulement de l'ordre de 1 à 2%. Pour ce derniers individus, les incubations de peau en présence de testostérone montrent l'existence d'une forte activité 11β-hydroxylase (23.8-25% pour le male, et 13% pour la femelle). Des différences liées au sexe sont observées de la même manière dans la production de métabolites 5α-réduits (environ 20% avec le tissu male et 13% avect le tissu femelle).

     

Gonadotrophin-releasing hormone agonist raises plasma concentrations of progestogens and enhances milt fluidity in male Atlantic halibut (Hippoglossus hippoglossus)

In two separate spawning seasons, spermiating male Atlantic halibut were implanted with pellets containing gonadotrophin-releasing hormone agonist (GnRHa). Males were bled repeatedly, and milt samples were collected. Blood samples were assayed for free and conjugated steroids: testosterone, 11-ketotestosterone, 17,20-dihydroxy-4-pregnen-3-one (17,20-P), 17,20-dihydroxy-4-pregnen-3-one (17,20-P), 17,20,21-trihydroxy-4-pregnen-3-one and steroids with a 17,20 configuration. Towards the end of the first season, pellets were implanted into three wild-caught and three hatchery-reared males. No control fish were available. The major progestogen in plasma was identified as sulphated 5-pregnane-3,17,20-triol (3,17,20-P-5-S). Concentrations of this steroid were stimulated by the GnRHa. Sulphated 17,20-P was also identified in the plasma, but at 10-fold lower concentrations than 3,17,20-P-5-S. In the middle of the second season, pellets were implanted into five hatchery-reared males; five unimplanted males were used as controls. Levels of androgens fell following GnRHa treatment, levels of progestogens rose briefly, and there was a significant increase in the fluidity of the milt. Of all the measured steroids, free and sulphated 17,20-P showed the best correlation with milt fluidity.     

Cortisol effects on the testicular androgen synthesizing capacity in common carp, Cyprinus carpio L.

Our previous studies on the effect of stress on pubertal development in carp have shown that repeated temperature changes caused an increase in cortisol levels and a retardation of the first waves of spermatogenesis. Identical effects, accompanied by a decrease in 11-ketotestosterone (11KT) plasma levels and the gonadosomatic index (GSI) were induced by cortisol administration via cortisol containing food pellets. The decrease in plasma 11KT is caused by a direct effect of cortisol on the steroid producing capacity of the testis, independent of luteinizing hormone (LH) levels. However, the mechanism through which cortisol interferes with testicular steroidogenesis is unknown. In the present study, we showed that in vitro physiological levels of cortisol can inhibit the conversion of 11β-hydroxyandrostenedione (OHA) into androstenetrione (OA), which is the precursor of 11KT, possibly by competing for the enzyme 11β-hydroxysteroid dehydrogenase (11β-HSD). The same mechanism may occur in vivo. However, our results demonstrate that an elevation of plasma cortisol levels during acute cortisol treatment did not result in lower plasma levels of OA and 11KT, but we did observe an accumulation of OHA. We suggest that the previously observed decrease in 11-oxygenated androgens, as an effect of long-term cortisol treatment, is caused by a retardation of testicular development. This results in a lower steroid synthesizing capacity of the testis as a whole. Although the in vitro observed cortisol inhibition of the conversion of OHA into 11KT plays a role in the accumulation of OHA, it apparently has no effect on the final 11KT plasma concentration. This revised version was published online in August 2006 with corrections to the Cover Date.     

Effect of androgens on seawater adaptation in Arctic char,Salvelinus alpinus

Sexually immature two-year old Arctic char (Salvelinus alpinus) were implanted with Silastic capsules containing testosterone or 11-ketoandrostenedione in early spring. Seawater adaptability of the hormone-treated and sham-operated fish was tested periodically from May to August using a 48h seawater challenge test with 25‰ seawater. The sham-operated control fish displayed a seasonal pattern in seawater adaptation, showing a good hypoosmoregulatory ability until mid June followed by a marked increase in plasma sodium and magnesium levels in July and August. Gill Na⁺-K⁺-ATPase activity decreased concurrently with the observed decrease in seawater adaptability. Over the same period the androgen-treated fish displayed a similar pattern in seawater adaptability, however, in May and June the plasma sodium levels were significantly higher in both androgen-treated groups compared to the control group. Plasma magnesium regulation was impaired in both androgen-treated groups in August. Gill Na⁺-K⁺-ATPase activity in the testosterone-treated fish was lower in June compared to the control fish, whereas the activity was not affected by 11-ketoandrostenedione treatment. The results show that while androgens impair the hypoosmoregulatory capacity in Arctic char, the seasonal pattern of seawater adaptability is not affected.     

Androgen levels and erythrocytosis in maturing brown trout,Salmo trutta L.

The number of circulating erythrocytes was monitored in two strains of brown trout during the spawning season. Erythrocyte numbers were significantly elevated in mature male fish of both strains compared with mature females or immature fish. This period of erythrocytosis coincided with elevated plasma 11-ketotestosterone levels in mature male fish, was out of phase with the testosterone peak in males and was not observed in females despite high levels of plasma testosterone. The results are discussed with reference to the control of erythropoiesis in higher vertebrates.