Contextual modulation of social and endocrine correlates of fitness: insights from the life history of a sex changing fish

Abstract

Steroid hormones are critical regulators of reproductive life history, and the steroid sensitive traits (morphology, behavior, physiology) associated with particular life history stages can have substantial fitness consequences for an organism. Hormones, behavior and fitness are reciprocally associated and can be used in an integrative fashion to understand how the environment impacts organismal function. To address the fitness component, we highlight the importance of using reliable proxies of reproductive success when studying proximate regulation of reproductive phenotypes. To understand the mechanisms by which the endocrine system regulates phenotype, we discuss the use of particular endocrine proxies and the need for appropriate functional interpretation of each. Lastly, in any experimental paradigm, the responses of animals vary based on the subtle differences in environmental and social context and this must also be considered. We explore these different levels of analyses by focusing on the fascinating life history transitions exhibited by the bi-directionally hermaphroditic fish, Lythrypnus dalli. Sex changing fish are excellent models for providing a deeper understanding of the fitness consequences associated with behavioral and endocrine variation. We close by proposing that local regulation of steroids is one potential mechanism that allows for the expression of novel phenotypes that can be characteristic of specific life history stages. A comparative species approach will facilitate progress in understanding the diversity of mechanisms underlying the contextual regulation of phenotypes and their associated fitness correlates.

Keywords: androgen; cortisol; parenting; reproduction; social status.

Figure 1

Reciprocal relationships between hormone, behavior, and fitness of an individual. The strength of relationship between any two factors can be modulated based on context and the environment in which the organism lives. The different shapes in (A) Environment 1 and (B) Environment 2 represent the role of context in modulating the bi-directional links between any two factors. The varying thickness of arrows represents the complexity of links between factors.

Figure 2

Simplified pathway of steroidogenesis in fish. Testosterone is converted to 11-Ketotestosterone (KT) via the sequential action of 11β-hydroxylase, which converts KT to 11β-hydroxytestosterone (11β-OHT), and 11β-hydroxysteroid dehydrogenase, which converts 11β-OHT to KT and cortisol to cortisone. Adapted from Pradhan et al. (2014c).

Figure 3

Life cycle of bluebanded gobies, Lythrypnus dalli, depicting the life history stages during the breeding season in waters off the coast of Santa Catalina Island, California. The dotted box encompasses the non-reproductive stages, which are not discussed in this review. The remainder are parts of the reproductive stages, and each of these comprise sub-stages of territorial aggression, dominance hierarchies, courtship (male jerks and female solicitation), spawning, and parenting. In the laboratory, social groups are easily set up under conditions that are permissive for natural sex change and for spawning. These fish also show alternative reproductive strategies to increase lifetime reproductive success, such as socially controlled bi-directional adult sex change and parasitic male morphs.

Figure 4

Integration of fitness and behavioral neuroendocrinology in Lythrypnus dalli. (A) Examples of fitness proxies that are commonly used to estimate reproductive success. One or more of these measures can be evaluated during different life history stages and within a particular endocrinological or social context. (B) Eggs at different stages of development, such as newly laid and eyed. (C) In stable social groups male reproductive success is negatively associated with the frequency of approaches and displacements in the social group (total approaches is male, alpha, beta, gamma approaches). Adapted from Solomon-Lane et al. (2014). (D) Intracerebroventricular (ICV) treatment of males presented females with a new social opportunity, permitting them to enter the nest and eat eggs. CBX, Carbenoxolone; KT, 11-ketotestosterone, ^*p < 0.05. Adapted from Pradhan et al. (2014c).

Figure 5

Proxies of steroid function at multiple levels of analysis. There are many different approaches to determine steroid levels in organisms. Steroids can be measured within particular tissues such as the brain, and in systemic circulation, such as plasma. Direct proxies within brain tissue include steroid signaling molecules such as receptors and steroidogenic machinery, such as enzymes (#1–8): 1, tissue; 2, membrane receptor protein; 3, synapse; 4, intracellular receptor protein; 5, steroid receptor mRNA expression; 6, steroidogenic enzyme mRNA expression; 7, steroidogenesis; 8, cerebrospinal fluid. Steroids can be synthesized in astroglia and within the the synaptic bouton (Saldanha et al., 2011). There are many proxies of systemic measures (#9–17): 9, plasma; 10, water-borne; 11, hair/fur; 12, feather; 13, saliva; 14, urine; 15, feces; 16; steroid metabolism; 17, steroid conjugation.

Figure 6

Endocrine context of Lythrypnus dalli, commonly used in the laboratory. (A) Steroid measurement proxies (B) Steroid manipulation approaches.

Figure 7

Social context of Lythrypnus dalli. (A) Stable social groups form a linear social hierarchy in the laboratory within 5 days. In the presence of the male, all females are in an environment inhibitory to sex change. (B) Sex change can then be readily induced in the alpha female by removing the male, which changes the social context. The most dominant female is now in a transitioning social environment that is permissive for sex change, while the subordinate females are in an environment inhibitory for sex change. Depending upon the specific group, there is substantial variation in the time over which a stable social hierarchy is re-established (“Dominance Phase”), after which there is a decline in rates of agonistic interactions.

Figure 8

Social context dependent effects of systemic (intraperitoneal) 11-ketotestosterone (KT) implants on agonistic interactions in Lythrypnus dalli. Alpha females were implanted with either KT or cholesterol and placed in a social environment that was permissive for sex change. (A) Alpha agonistic efficiency (AgEf) (displacements/approaches) toward betas relative to time after implant. Alpha females implanted with cholesterol had a decline in agonistic efficiency during the Dominance Phase (represented by dotted lines), but had dramatically higher agonistic efficiency the following day. (B) Beta Agonistic efficiency toward alphas relative to time after implant (n = 8 Chol and n = 10 KT). (C) Categorical representation of rates of beta approaches when alpha agonistic efficiecy was < or > 0.5. The numbers above bars represent the number of groups for each category. The inset is a regression of alpha agonistic efficiecy against rates of betas approaching alphas after alphas were treated with either KT or Cholesterol (N = 15). Note that some individuals were excluded from this analysis due to zero rates of interaction and overlap does not allow all data points to be seen clearly, ^*p < 0.05.

Figure 9

Functional interpretation of endocrine studies should be cognizant of the relevant proxy. Loose links exist, such that expression of phenotype is dependent upon both, (A) Endocrine and (B) Social factors. (C) Balance between these two factors is necessary for the regulation of function and increase lifetime reproductive success. (D) Several endocrine and social context factors must be considered when designing experiments.