Interacting effects of environmental enrichment across multiple generations on early life phenotypes in zebrafish

This is the peer reviewed version of the following article: [Green, M. R., & Swaney, W. T. (2023). Interacting effects of environmental enrichment across multiple generations on early life phenotypes in zebrafish. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution, 340(5), 354-365], which has been published in final form at [https://doi.org/10.1002/jez.b.23184]. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. This article may not be enhanced, enriched or otherwise transformed into a derivative work, without express permission from Wiley or by statutory rights under applicable legislation. Copyright notices must not be removed, obscured or modified. The article must be linked to Wiley’s version of record on Wiley Online Library and any embedding, framing or otherwise making available the article or pages thereof by third parties from platforms, services and websites other than Wiley Online Library must be prohibited.The environment plays an important role in an individual's development during early life, however, parents may also influence offspring development through so called “parental effects.” We examined the effects of environmental enrichment in zebrafish (Danio rerio) across two generations through the paternal lineage. Fathers and grandfathers were exposed to either standard or high levels of housing enrichment for 4-weeks during adulthood. First-generation (F1) and second-generation (F2) offspring were obtained from controlled breeding and tested as larvae for changes in morphology at hatching stage (72hpf), and in locomotor activity at larval stage (120hpf) in both generations. We found paternal experience of enrichment resulted in changes in trunk length of F1 offspring and changes in spine curvature and dorsal length of F2 offspring, while changes in snout morphology of F2 offspring seemed to be driven by whether grandpaternal and paternal experience of the environment was matched or not. We found that while paternal enrichment increased the frequency of spontaneous movement in F1 and F2 offspring, interacting effects of paternal and grandpaternal enrichment on movement distance were seen in F2 offspring, and that spontaneous movement and the distance that larvae swam are thus distinct phenotypes that were differentially affected by the experiences of previous paternal generations. Taken together, these findings suggest that the parental and grandparental environment influence zebrafish behavior and morphology. The nature of these effects and the design of this study mean that these phenotypes were likely the result of nongenetic transmission through the paternal germline

Demasculinization of male guppies increases resistance to a common and harmful ectoparasite

Parasites are detrimental to host fitness and therefore should strongly select for host defence mechanisms. Yet, hosts vary considerably in their observed parasite loads. One notable source of inter-individual variation in parasitism is host sex. Such variation could be caused by the immunomodulatory effects of gonadal steroids. Here we assess the influence of gonadal steroids on the ability of guppies (Poecilia reticulata) to defend themselves against a common and deleterious parasite (Gyrodactylus turnbulli). Adult male guppies underwent 31 days of artificial demasculinization with the androgen receptor-antagonist flutamide, or feminization with a combination of flutamide and the synthetic oestrogen 17 β-estradiol, and their parasite loads were compared over time to untreated males and females. Both demasculinized and feminized male guppies had lower G. turnbulli loads than the untreated males and females, but this effect appeared to be mainly the result of demasculinization, with feminization having no additional measurable effect. Furthermore, demasculinized males, feminized males and untreated females all suffered lower Gyrodactylus-induced mortality than untreated males. Together, these results suggest that androgens reduce the ability of guppies to control parasite loads, and modulate resistance to and survival from infection. We discuss the relevance of these findings for understanding constraints on the evolution of resistance in guppies and other vertebrates

Nonapeptide influences on social behaviour: effects of vasotocin and isotocin on shoaling and interaction in zebrafish

Nonapeptides are important regulators of social behaviour across vertebrate taxa. While their role in simple grouping behaviour has been explored in estrildid finches, other taxa are understudied, prompting us to investigate nonapeptide influences on shoaling behaviour in zebrafish. Subjects received injections of isotocin, an isotocin antagonist, vasotocin, a vasotocin antagonist, or saline, followed by a test of grouping behaviour. Vasotocin decreased social interaction with the shoal. Unexpectedly, the vasotocin antagonist also reduced social interaction with the shoal, as well as general shoaling behaviour. Isotocin and its antagonist had minimal effects on grouping behaviours. These results suggest social interaction and shoaling are discrete aspects of sociality differentially influenced by vasotocin, although we cannot discount possible anxiogenic effects of vasotocin. Contrasting these results with studies in other systems demonstrates that each nonapeptide’s role in social behaviour varies across taxa, and cautions against a simplistic characterisation of nonapeptides as prosocial regulators of behaviour

Sexual experience affects reproductive behavior and preoptic androgen receptors in male mice

Reproductive behavior in male rodents is made up of anticipatory and consummatory elements which are regulated in the brain by sensory systems, reward circuits and hormone signaling. Gonadal steroids play a key role in the regulation of male sexual behavior via steroid receptors in the hypothalamus and preoptic area. Typical patterns of male reproductive behavior have been characterized, however these are not fixed but are modulated by adult experience. We assessed the effects of repeated sexual experience on male reproductive behavior of C57BL/6 mice; including measures of olfactory investigation of females, mounting, intromission and ejaculation. The effects of sexual experience on the number of cells expressing either androgen receptor (AR) or estrogen receptor alpha (ERα) in the primary brain nuclei regulating male sexual behavior was also measured. Sexually experienced male mice engaged in less sniffing of females before initiating sexual behavior and exhibited shorter latencies to mount and intromit, increased frequency of intromission, and increased duration of intromission relative to mounting. No changes in numbers of ERα-positive cells were observed, however sexually experienced males had increased numbers of AR-positive cells in the medial preoptic area (MPOA); the primary regulatory nucleus for male sexual behavior. These results indicate that sexual experience results in a qualitative change in male reproductive behavior in mice that is associated with increased testosterone sensitivity in the MPOA and that this nucleus may play a key integrative role in mediating the effects of sexual experience on male behavior

C-tactile afferents: Cutaneous mediators of oxytocin release during affiliative tactile interactions?

Low intensity, non-noxious, stimulation of cutaneous somatosensory nerves has been shown to trigger oxytocin release and is associated with increased social motivation, plus reduced physiological and behavioural reactivity to stressors. However, to date, little attention has been paid to the specific nature of the mechanosensory nerves which mediate these effects. In recent years, the neuroscientific study of human skin nerves (microneurography studies on single peripheral nerve fibres) has led to the identification and characterisation of a class of touch sensitive nerve fibres named C-tactile afferents. Neither itch nor pain receptive, these unmyelinated, low threshold mechanoreceptors, found only in hairy skin, respond optimally to low force/velocity stroking touch. Notably, the speed of stroking which c-tactile afferents fire most strongly to is also that which people perceive to be most pleasant. The social touch hypothesis posits that this system of nerves has evolved in mammals to signal the rewarding value of physical contact in nurturing and social interactions. In support of this hypothesis, in this paper we review the evidence that cutaneous stimulation directly targeted to optimally activate c-tactile afferents reduces physiological arousal, carries a positive affective value and, under healthy conditions, inhibits responses to painful stimuli. These effects mirror those, we also review, which have been reported following endogenous release and exogenous administration of oxytocin. Taken together this suggests C-tactile afferent stimulation may mediate oxytocin release during affiliative tactile interactions

README

This file explains all of the variables in each of the datasets that accompany: Cabrera-Álvarez, María J., Swaney, William T., Reader, Simon M. (2017) Forebrain activation during social exposure in wild-type guppies. Physiology & Behaviour 182, 107-113