Dads matter: causes and consequences of plasticity in paternal care

Stein, Laura Renee

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https://hdl.handle.net/2142/88251 Copy

Description

Title

Dads matter: causes and consequences of plasticity in paternal care

Author(s)

Stein, Laura Renee

Issue Date

2015-06-19

Director of Research (if dissertation) or Advisor (if thesis)

Bell, Alison M.

Doctoral Committee Chair(s)

Bell, Alison M.

Committee Member(s)

• Fuller, Rebecca C.
• Cheviron, Zachary A
• Mahoney, Megan M.

Department of Study

School of Integrative Biology

Discipline

Biology

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

• behavioral type
• behavioral syndrome
• personality
• parenting
• fathering
• paternal care
• parental effects
• transgenerational plasticity
• flexible stem
• stickleback

Abstract

Whether phenotypic plasticity can accelerate evolution is often debated. Transgenerational plasticity (parental effects) are a particularly potent form of plasticity that occurs when the environment experienced by a parent influences offspring phenotypes, and theory suggests that parental effects can increase the speed of directional evolution. Parental effects might facilitate adaptation to new environments if parents are capable of ‘programming’ their offspring for the type of environment they are likely to experience. Therefore, it is possible that plasticity in one generation (changes in parental behavior, for example) might influence offspring in the next generation and may facilitate adaptive evolution and the colonization of novel environments, yet these ideas remain largely untested empirically. In a wide range of organisms, including humans, mothers’ experiences can affect offspring morphology, physiology, and behavior. There is also an emerging literature showing that the way mothers behave toward their offspring can have a long-lasting influence on their offspring. Comparatively, a relatively unexplored possibility is that in species with paternal care, fathers adjust their parenting in response to stressors, and adjustments in care have long-term consequences for offspring (as has been shown for mothers). Here, I report a series of studies examining how plasticity in father behavior might facilitate rapid adaptation in threespine stickleback fish (Gasterosteus aculeatus) via paternal effects. In threespine stickleback, the father is the sole provider of parental care, and parental care is necessary for offspring survival; without parental defense, nests would be depredated. As males are the sole provider of care, it is possible to separate post-fertilization paternal effects due to variations in paternal behavior from maternal effects. Parental behaviors include oxygenating eggs via fanning with pectoral fins and retrieving offspring. In stickleback, the marine ancestral form is extant and is thought to have remained relatively unchanged. Multiple independently-derived freshwater populations have repeatedly diverged from this ancestral marine form, resulting in numerous replicates of derived populations, many of which are locally adapted. Therefore, the threespine stickleback system provides a good model for examining causes and consequences of plasticity in paternal behavior in response to predation risk. First, I assessed the impact of the experience of parenting on a parent’s behavior and physiology. While there is a rich literature documenting physiological and behavioral changes that organisms undergo as they become parents, there are little data in either humans or nonhuman animals that test the intuitive hypothesis that becoming a parent influences personality traits (behaviors that are variable among individuals and consistent within individuals over time). Life history theory predicts that males should be less risk-averse after successfully parenting, and the neuroendocrinology of parenting suggests that parenting could reorganize the hormonal landscape and behavior of fathers. Using a controlled longitudinal study, I randomly assigned males to either the experimental (reproduced and parented) or control (did not reproduce and parent) group, and repeatedly measured a personality trait (‘boldness’) and 11-ketotestosterone (11-kT, the major androgen in fishes) in individual males. In the control group, males became more bold over time. However, in the experimental group, boldness did not change. Further, 11-kT changed dramatically in the experimental group, and changes in 11-kT in parents were associated with boldness after parenting ceased. Further, males that parented showed greater among-individual variation in 11-kT, suggesting a potential mechanism driving natural variation in parenting behavior. This study is one of the first to test proximate and ultimate explanations for changes in personality as a function of a major adult event – reproduction and parenting. Second, I examined plasticity in paternal behavior in both the lab and field. Using a within-subject design, I randomly assigned wild-caught males from Putah Creek, CA to either the “predator-exposed” or “unexposed” treatment group and allowed them to spawn. Three days post-fertilization, I introduced a model rubber sculpin (a fish predator present in Putah Creek) into the tank of “predator-exposed” males for two minutes. Males in the “unexposed” treatment did not experience the predator. Males were then allowed to parent normally and complete their clutch. I then moved males into new tanks and males that were initially in the “predator-exposed” treatment were assigned to the “unexposed” treatment, and vice versa. I found that males exhibited natural variation in parenting behavior, and consistently differed from one another both within and across clutches. Further, males exposed to predation risk reduced fanning behavior for two days, and then resumed normal fanning for the remainder of the nesting cycle. This demonstrated that males plastically adjusted their parenting behavior in the presence of a predator. I also examined plasticity in parenting behavior in the field. I marked parenting males in the Navarro River, CA that had eggs in the nest with flags. I measured undisturbed parenting behavior, and then I presented males with a caged live gravid female (representing courtship opportunity), a live conspecific male (representing territorial intrusion), and a live sculpin (representing predation risk), with one hour between each stimuli. I found that males showed natural variation and consistently differed from one another in parenting behavior as in the lab. Males also exhibited behavioral plasticity by reducing fanning while stimuli were present. Further, I found that males that were more attentive to the stimuli fanned the nest more often, suggesting the presence of a behavioral syndrome. I then assessed the consequences of fathers’ plasticity by examining the impact of parental experience with predation risk on offspring phenotypes. I compared the morphology, behavior, and physiology of adult offspring that were reared by fathers that either had or had not been exposed to predation risk during the time when they were providing care. I found that offspring of predator exposed fathers were smaller, in worse body condition, showed duller nuptial coloration, and were less active than offspring of unexposed fathers. Fathers’ experience with predation risk also induced a sex-based difference in cortisol concentration, such that daughters had higher cortisol than sons in response to predation risk (offspring of unexposed fathers showed no difference in cortisol concentration between sons and daughters). These phenotypes matched those of stickleback from high-predation populations and juvenile stickleback exposed to predator cues. These results suggest that fathers might be capable of ‘programming’ their offspring for living in a high predation environment via short-term adjustments in paternal behavior in response to immediate predation risk. Finally, I tested the hypothesis that behavioral plasticity by fathers in response to predation risk might have facilitated the adaptive radiation of threespined sticklebacks by comparing plastic responses in marine and freshwater populations. In freshwater, major predators on stickleback fry and juveniles are Odonate (dragonfly) larvae, a predator that is not present in marine populations, and which exerts important selective pressure on stickleback morphology. I collected fish from nine populations: two marine (ancestral), three freshwater of known age (2-30 generations, “new” freshwater), and four established freshwater. I induced plasticity in fathers by exposing them to a predator found only in freshwater. While derived populations showed antipredator responses, ancestral populations did not. When compared across populations, plasticity increased with population age (and thus predator familiarity). Finally, I found greater variation in plastic responses in ancestral populations compared to derived populations. Altogether, my results suggest that, rather than ancestral populations showing greater overall levels of plasticity than derived populations, ancestral populations instead show greater standing variation in behavioral reaction norms, potentially providing different trajectories on which selection can then act. Taken together, these studies provide a comprehensive view of how plasticity both within and across generations can influence evolutionary patterns.

Graduation Semester

2015-8

Type of Resource

text

Permalink

http://hdl.handle.net/2142/88251

Copyright and License Information

Copyright 2015 Laura Stein

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