Introduction
Parental effects occur when maternal, paternal or both parental
phenotypes affect offspring phenotypes
(Bonduriansky & Day 2018;
Uller et al. 2013). Such effects
occur in a wide range of taxa (Uller
2008) via different pre- and post-natal routes (e. g. microhabitat
selection for eggs, reproductive investment, intrauterine environment,
parental care). Parental experiences can affect offspring fitness
(Burton & Metcalfe 2014), although are
not necessarily adaptive (Bonduriansky &
Day 2018). For example, maternal undernourishment is associated with
the development of diabetes and obesity in the progeny
(Hales & Barker 2001), while paternal
undernutrition in mice results in altered glucose metabolism and growth
in the offspring (Anderson et al.2006).
The knowledge about the molecular mechanisms of the pre-natal parental
effects is still limited (Gluckmanet al. 2005; Jensen et al.2014). The transmission of some parental effects via germline has been
related to genetic mechanisms, such as the association between the
frequency of some deleterious mutations in sperm and increasing male’s
age (Wyrobek et al. 2006).
However, it is likely that non-genetic mechanisms also play a major role
in parent-offspring information transfer
(Danchin et al. 2011;
Jablonka & Raz 2009), as genetic-based
inheritance solely cannot fully explain the variation of offspring
phenotypes (Danchin et al. 2011).
Epigenetic modifications, such as DNA methylation, histone modifications
and microRNAs, mediate rapid changes in transcription influenced by
environmental changes (Richards 2006)
that can affect phenotypes (Richardset al. 2017; Verhoeven et
al. 2016). Among the epigenetic mechanisms, DNA methylation is the
best characterized, being important on several biological processes,
from genomic imprinting to cell differentiation
(Jones 2012;
Lea et al. 2017). DNA methylation
on regulatory regions generally supresses gene expression
(Moore et al. 2013), whereas
methylation in gene bodies contributes to reducing transcriptional noise
(Huh et al. 2013). Thus,
differential methylation can affect gene expression and result in
phenotypic plasticity (Baerwald et
al. 2016; Herman & Sultan 2016).
However, while the transmission of environmentally-induced epialleles
via DNA methylation from parents to offspring has been identified in
plants, whether epigenetic mechanisms can provide a heritable memory of
environmental influence in animals remains controversial
(Heard & Martienssen 2014), as well as
the potential adaptive value of this type of transmission
(Perez & Lehner 2019).
The parental rearing environment can induce phenotypic modifications
during early development which can be long-lasting and potentially
intergenerational (Burton & Metcalfe
2014). A well known example is the effect of structural environmental
complexity on behaviour (Braithwaite &
Salvanes 2005; Roberts et al.2011), physiology (Näslund et al.2013), cognitive capacity (Salvaneset al. 2013) and brain structure
(Kihslinger et al. 2006) in fish.
Physical structures are critical for most fish at different points of
their life cycle (e. g. for spawning, sheltering, foraging), suggesting
that structural complexity is an important ecological factor of their
natural environment (Näslund & Johnsson
2016). Captive fish reared in enriched environments have shown
increased survival in the wild compared to those reared in impoverished
environments (D’Anna et al. 2012;
Roberts et al. 2014), as well as
enhanced cognitive capacity and behavioural flexibility
(Salvanes et al. 2013;
Spence et al. 2011;
Strand et al. 2010). However,
little is known about the molecular mechanisms underlying plastic
responses to environmental enrichment, or whether these changes could be
transmitted across generations (Näslundet al. 2012; Näslund & Johnsson
2016).
Kyrptolebias marmoratus (Poey 1880) is a predominantly
self-fertilising fish living in mangrove forests in North and Central
America (Tatarenkov et al. 2017),
occupying a varied range of mangrove fossorial microhabitats influenced
by periodical tide variation (Ellisonet al. 2012b). Its naturally inbred nature makes K.
marmoratus populations particularly suited to assess the influence of
the environment on behaviour (Ellisonet al. 2013; Ellison et al.2012b), phenotypic plasticity (Earleyet al. 2012) and epigenetics
(Ellison et al. 2015). In their
natural environment, the species inhabits inherently heterogenous
mangrove habitats, with different selfing lineages coexisting in the
same microhabitat (Ellison et al.2012b), and displays aggression towards conspecifics
(Taylor 2000) that vary depending on
kinship relationship (Edenbrow & Croft
2012; Ellison et al. 2013). These
fish ermerse to forage or in response to intraspecific aggression or
poor water quality (Turko et al.2011), suggesting that environmental complexity may play an important
role on their ecology and behaviour.
We reared two generations of
genetically-identical K. marmoratus in matched and mismatched
environments with different levels of structural complexity to examine
the intergenerational influence of environmental enrichment on
individual physiology and behaviour,
and the potential role of
epigenetic mechanisms (brain DNA methylation) to mediate
environmentally-induced parental effects.