Trans-generational responses to low pH depend on parental gender in a calcifying tubeworm

Abstract

The uptake of anthropogenic CO2 emissions by oceans has started decreasing pH and carbonate ion concentrations of seawater, a process called ocean acidification (OA). Occurring over centuries and many generations, evolutionary adaptation and epigenetic transfer will change species responses to OA over time. Trans-generational responses, via genetic selection or trans-generational phenotypic plasticity, differ depending on species and exposure time as well as differences between individuals such as gender. Males and females differ in reproductive investment and egg producing females may have less energy available for OA stress responses. By crossing eggs and sperm from the calcareous tubeworm Hydroides elegans (Haswell, 1883) raised in ambient (8.1) and low (7.8) pH environments, we observed that paternal and maternal low pH experience had opposite and additive effects on offspring. For example, when compared to offspring with both parents from ambient pH, growth rates of offspring of fathers or mothers raised in low pH were higher or lower respectively, but there was no difference when both parents were from low pH. Gender differences may result in different selection pressures for each gender. This may result in overestimates of species tolerance and missed opportunities of potentially insightful comparisons between individuals of the same species.

The other 96%: Can neglected sources of fitness variation offer new insights into adaptation to global change?

“…For instance, Donelson, Munday, McCormick, and Pitcher (2012) found that damselfish ( Acanthochromis polyacanthus ) exposed to thermal stress produce offspring with superior thermal tolerance relative to offspring of unexposed parents. Other studies, however, have shown that stressful parental environments can lower offspring quality (Guillaume, Monro, & Marshall, 2016; Huxman et al., 1998; Lane, Campanati, Dupont, & Thiyagarajan, 2015; Shama & Wegner, 2014). In our study, maternal environmental effects on survival were unlikely to have been caused by past environmental conditions, as all mothers came from the same collection site and were acclimatized before use.…”

Can multi-generational exposure to ocean warming and acidification lead to the adaptation of life-history and physiology in a marine metazoan?

“…For example, parental exposure to ocean acidification increases the rate of juvenile development in the Sydney rock oyster, Saccostrea glomerata (Parker et al, 2012), but decreases developmental rate in G. aculeatus (Schade et al, 2014). The relationship is further complicated in the marine tubeworm Hydroides elegans, whose offspring grow twice as fast if the fathers have been exposed to ocean acidification but 25% slower if the mothers experience the same conditions (Lane et al, 2015). As both the males and females were exposed to ocean acidification in this study, it is possible that the neutral response that we observed in F2, F4 and F6 are driven by opposite, additive effects of the parental environment experienced.…”

“…Several transgenerational studies have measured the effect of ocean acidification on juvenile development (Parker et al, 2012;Schade et al, 2014;Lane et al, 2015), but no pattern is evident in the results. For example, parental exposure to ocean acidification increases the rate of juvenile development in the Sydney rock oyster, Saccostrea glomerata (Parker et al, 2012), but decreases developmental rate in G. aculeatus (Schade et al, 2014).…”

“…However, there have been no multi-driver, multigenerational studies in marine organisms, so it is unclear whether a similar pattern will emerge when ocean warming and acidification are combined, and this is one avenue of research that must be pursued. Single-driver experiments reveal that benefits are likely to be retained over multiple generations via alterations in parental resource partitioning (Marshall and Uller, 2007;Lane et al, 2015) and somatic factors such as antibiotics, antioxidants, hormones and mitochondria (Hamdoun and Epel, 2007;De Wit et al, 2016;Shama et al, 2016), although epigenetic effects on protein conformation, DNA methylation and chromatin marks may also play a role (Jablonka and Raz, 2009;Bonduriansky et al, 2012;Veilleux et al, 2015;Munday et al, 2017;Putnam et al, 2016).…”

Does sex really matter? Explaining intraspecies variation in ocean acidification responses

“…However, despite recent evidence that many physiological, behavioural, immunological, molecular and neuro-toxicological functions are influenced by sex-based differences [9,10], and despite many of these same processes being impacted by elevated pCO 2 [5], the overarching role of sex in determining response to OA remains understudied [11]. Here, we employ a systematic map approach: a transparent, robust and repeatable method to identify and collect relevant literature to answer the question of how sex is considered within experimental OA research [12].…”