Parents exposed to warming produce offspring lower in weight and condition

Abstract

The parental environment can alter offspring phenotypes via the transfer of non‐genetic information. Parental effects may be viewed as an extension of (within‐generation) phenotypic plasticity. Smaller size, poorer physical condition, and skewed sex ratios are common responses of organisms to global warming, yet whether parental effects alleviate, exacerbate, or have no impact on these responses has not been widely tested. Further, the relative non‐genetic influence of mothers and fathers and ontogenetic timing of parental exposure to warming on offspring phenotypes is poorly understood. Here, we tested how maternal, paternal, and biparental exposure of a coral reef fish ( Acanthochromis polyacanthus ) to elevated temperature (+1.5°C) at different ontogenetic stages (development vs reproduction) influences offspring length, weight, condition, and sex. Fish were reared across two generations in present‐day and projected ocean warming in a full factorial design. As expected, offspring of parents exposed to present‐day control temperature that were reared in warmer water were shorter than their siblings reared in control temperature; however, within‐generation plasticity allowed maintenance of weight, resulting in a higher body condition. Parental exposure to warming, irrespective of ontogenetic timing and sex, resulted in decreased weight and condition in all offspring rearing temperatures. By contrast, offspring sex ratios were not strongly influenced by their rearing temperature or that of their parents. Together, our results reveal that phenotypic plasticity may help coral reef fishes maintain performance in a warm ocean within a generation, but could exacerbate the negative effects of warming between generations, regardless of when mothers and fathers are exposed to warming. Alternatively, the multigenerational impact on offspring weight and condition may be a necessary cost to adapt metabolism to increasing temperatures. This research highlights the importance of examining phenotypic plasticity within and between generations across a range of traits to accurately predict how organisms will respond to climate change.

Timing specific parental effects of ocean warming in a coral reef fish

“…Accordingly, we observed in this experiment that offspring developmental temperature had a significant effect on their own body condition only when their parents developed and reproduced at ambient temperature, with the parental thermal exposure otherwise controlling offspring length and weight ratio (Spinks et al, 2022). The consistency between parental and offspring thermal exposures did not affect offspring condition (Spinks et al, 2022) or molecular responses, suggesting carry-over rather than anticipatory parental effects (Bonduriansky & Crean, 2018; Uller et al, 2013). On the contrary, mismatches between the temperatures experienced by the two parents at development or across parental lifespan played an important role in shaping offspring thermal acclimation.…”

“…In order to investigate the importance of exposure timing in the response to warming, we analysed liver gene expression of A. polyacanthus exposed to elevated temperature over two generations. Detailed descriptions of the experimental set-up are provided in Spinks et al (2021; 2022). Briefly, adult spiny chromis damselfish (F0 generation) were collected from the wild in the Palm Islands region (18°37′ S, 146°30′ E) and nearby Bramble Reef (18°22′S, 146°40′E) of the central Great Barrier Reef in Australia, paired and housed with seasonally cycling water temperature resembling the collection site conditions.…”

“…1), which followed the above-mentioned seasonal and diurnal cycles of water temperature. During rearing, approximately 9% natural mortality occurred (Spinks et al, 2022). At 80 days post-hatching (dph), F2 fish were sexed by external examination of their urogenital papilla, and two males and two females per clutch per treatment (twelve to twenty individual fish per treatment; Suppl.…”

“…Elevated temperature exposure at reproduction caused low reproductive output and poor hatchling quality (Spinks et al, 2021). At 80 days post-hatching, offspring from parents that reproduced at elevated temperature were still in poorer body condition compared to offspring from control parents, regardless of the parental and of the offspring’s own developmental thermal environment (Spinks, Donelson, Bonzi, Ravasi, & Munday, 2022). Additionally, parental exposure to elevated temperature at development also resulted in lower 80-day old offspring condition.…”

Incorporating egg-transporting pathways into conservation plans of spawning areas: An example of small yellow croaker (Larimichthys polyactis) in the East China Sea zone

“…The water temperatures that address the thermal limits of reproduction provide physiological switches for the beginning and cessation of fish reproduction. Temperature can directly affect the initiation of spawning by promoting and inhibiting hormone synthesis, but the warmer temperature may cause the cessation of fish reproduction and a shorter spawning period (Motani and Wainwright, 2015;Spinks et al, 2021). A recent comparative study on fish identified that spawning adults and embryos had narrower thermal tolerance ranges, as reproduction and embryogenesis were the most thermally sensitive time for fishes (van Heerwaarden and Sgrò, 2021).…”