Sources of individual variation in plasma testosterone levels

Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, PO Box 1564, 82305 Seewiesen, Germany.
Philosophical Transactions of The Royal Society B Biological Sciences (Impact Factor: 7.06). 06/2008; 363(1497):1711-23. DOI: 10.1098/rstb.2007.0001
Source: PubMed


The steroid hormone testosterone (T) plays a central role in the regulation of breeding in males, because many physiological, morphological and behavioural traits related to reproduction are T dependent. Moreover, in many seasonally breeding vertebrates, male plasma T levels typically show a pronounced peak during the breeding season. While such population-level patterns are fairly well worked out, the sources and the implications of the large variability in individual T levels within the seasonal cycle remain surprisingly little understood. Understanding the potential sources of individual variation in T levels is important for behavioural and evolutionary ecologists, for at least two reasons. First, in 'honest signalling' theory, T is hypothesized to play a critical role as the assumed factor that enforces honesty of the expression of sexually selected quality indicators. Second, T is often considered a key mediator of central life-history trade-offs, such as investment in survival versus reproduction or in mating versus parental care. Here, we discuss the patterns of within- and between-individual variation in male plasma T levels in free-living populations of birds. We argue that it is unclear whether this variability mainly reflects differences in underlying individual quality (intrinsic factors such as genetic or maternal effects) or in the environment (extrinsic factors including time of day, individual territorial status and past experience). Research in avian behavioural endocrinology has mainly focused on the effects of extrinsic factors, while other sources of variance are often ignored. We suggest that studies that use an integrative approach and investigate the relative importance of all potential sources of variation are essential for the interpretation of data on individual plasma T levels.

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    • "Testosterone regulates a variety of male reproductive characteristics, such as the development of primary (Kempenaers et al., 2008) and secondary sexual characteristics (Buchanan et al., 2003), courtship, and aggression towards conspecific males (Hegner and Wingfield, 1987; Landys et al., 2010). "
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    ABSTRACT: Energy deficiency can suppress reproductive functions in vertebrates. As the orchestrator of reproductive function, endocrine activity of the hypothalamo-pituitary-gonadal (HPG) axis is potentially an important mechanism mediating such effects. Previous experiments in wild-caught birds found inconsistent relationships between energy deficiency and seasonal reproductive function, but these experiments focused on baseline HPG axis activity and none has investigated the responsiveness of this axis to endocrine stimulation. Here, we present data from an experiment in Abert's Towhees, Melozone aberti, using gonadotropin-releasing hormone (GnRH) and luteinizing hormone (LH) challenges to investigate whether energy deficiency modulates the plasma testosterone (T) responsiveness of the HPG axis. Wild-caught birds were either ad libitum-fed or energetically constrained via chronic food restriction during photoinduced reproductive development. Energy deficiency did not significantly affect the development of reproductive morphology, the baseline endocrine activity of the HPG axis, or the plasma T response to GnRH challenge. Energy deficiency did, however, decrease the plasma T responsiveness to LH challenge. Collectively, these observations suggest that energy deficiency has direct gonadal effects consisting in decreased responsiveness to LH stimulation. Our study, therefore, reveals a mechanism by which energy deficiency modulates reproductive function in wild birds in the absence of detectable effects on baseline HPG axis activity. © 2015. Published by The Company of Biologists Ltd.
    Journal of Experimental Biology 07/2015; 218(17). DOI:10.1242/dev.123042 · 2.90 Impact Factor
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    • "It is noteworthy that T males showed considerable variation in their cortisol and 11-KT plasma levels. This could be the result of intrinsic variability among fish (Kempenaers et al., 2008; Williams, 2008), differences in the readiness to spawn at the time of fish analysis (Kindler et al., 1989; Liley et al., 1986; Scott et al., 1984), but also due to the heterogeneous social environment each fish experienced (DeVries et al., 2003; Oliveira, 2004). As we could not distinguish between male and female C. dimerus, all experimental setups possibly differed in the proportion of sexes. "
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    ABSTRACT: Social animals with hierarchal dominance systems are particularly susceptible to their social environment. There, interactions with conspecifics and hierarchal position can greatly affect an individual's behavior, physiology and reproductive success. Our experimental model, Cichlasoma dimerus, is a serially-monogamous Neotropical cichlid fish with a hierarchical social system, established and sustained through agonistic interactions. In this work, we aimed to describe C. dimerus social structure and its association with hormonal profiles and testicular cellular composition. We recorded and quantified agonistic interactions from the territorial pair, i.e. the top ranked male and female, and the lowest ranked male of stable social groups. Plasma levels of 11-ketotestosterone (11-KT), testosterone, 17β-estradiol (E2) and cortisol were measured by ELISA. Results show that territorial pairs cooperatively guarded the territory, but rarely attacked in synchrony. Territorial males had higher testosterone and 11-KT plasma levels than non-territorial males, while E2 and an index of its metabolization from testosterone were higher in non-territorial males. No difference was observed in cortisol levels. Plasma 11-KT and an index of the conversion of testosterone to 11-KT, positively correlated with the frequency of aggressiveness, while E2 showed the opposite pattern. Territorial males had a higher gonadosomatic index than non-territorial males. The quantification of testicular cellular types revealed that the percentage of spermatocytes and spermatids were higher in non-territorial males, while territorial males showed a greater percentage of spermatozoa. Thus, C. dimerus male social position within a stable hierarchy is associated with distinct behaviors, steroid levels and testicular degree of development. Copyright © 2015. Published by Elsevier Inc.
    Hormones and Behavior 01/2015; 69. DOI:10.1016/j.yhbeh.2015.01.008 · 4.63 Impact Factor
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    • "Body-mass development was monitored by weighing the individuals approximately once per week using an electronic balance (accurate to 60.1 g). For monitoring male maturity and breeding condition (Barkley and Goldman 1977, Fail and Whitsett 1988, Kempenaers et al. 2008 "
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    ABSTRACT: In seasonal environments, the optimal onset of reproduction plays a major role in defining the reproductive success of an individual. Environmental cues, like day length, weather conditions, and food, regulate the initiation and termination of the breeding season. Besides the interspecific variation in response to environmental cues, it has been suggested that due to different selection pressures, females and males can have different responses to environmental stimuli. However, this phenomenon has gained relatively little consideration, and the physiological mechanism behind these differences is not well known. Here, we report how two different environmental cues, variability of temperature and nutritional conditions in spring, affect the onset of breeding in a boreal small rodent, the bank vole, Myodes glareolus. We exposed wild-trapped individuals to four different treatments manipulating temperature (stable vs. variable) and food quality (high vs. low protein content) over five weeks in the laboratory. We monitored body-mass development, food consumption, and initiation of breeding. We found sex-specific responses to temperature variability, as males achieved their breeding condition faster in variable temperature treatments, whereas female maturation was delayed. Food quality had no effect on the onset of breeding. To test for possible reproductive trade-offs caused by reproductive decisions made in early spring, the experiment was continued in large outdoor enclosures. There seemed to be no significant long-term effects on reproduction, but early summer survival was affected by climate conditions experienced in spring. Our results show clear sex differences in the response to environmental cues regulating the onset of reproduction in bank voles. Hence, our study suggests that when an organism experiences rapid environmental changes, as are occurring on a global scale, divergent cues may lead to a reproductive mismatch between the sexes. This could noticeably decrease the fitness of many seasonally breeding species.
    Ecology 10/2014; 95(10):2851–2859. · 4.66 Impact Factor
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