Plastic adjustments of biparental care behavior across embryonic development under elevated temperature in a marine ectotherm

Spatafora, Davide; N’Siala, Gloria Massamba; Quattrocchi, Federico; Milazzo, Marco; Calosi, Piero

doi:10.1002/ece3.7902

Cited by 3 publications

(3 citation statements)

References 86 publications

(143 reference statements)

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“…When parents reproduced at +1.5°C, newly hatched offspring were either shorter or lighter, which is not surprising given embryos developed in the same elevated temperature as their parents and warming can increase metabolic and developmental rates (Sheridan & Bickford, 2011 ; Spinks et al, 2021 ). Alternatively, smaller hatchlings may be the result of stressed parents devoting less energy to embryonic care (Spatafora et al, 2021 ; Wiley & Ridley, 2016 ). Nevertheless, by three months post‐hatching it did not seem to matter whether parents had been exposed to higher temperature during development or reproduction; offspring were lower in weight and condition.…”

Section: Discussionmentioning

confidence: 99%

Parents exposed to warming produce offspring lower in weight and condition

Spinks

Donelson

Bonzi

et al. 2022

Ecology and Evolution

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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.

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Section: Discussionmentioning

confidence: 99%

Parents exposed to warming produce offspring lower in weight and condition

Spinks

Donelson

Bonzi

et al. 2022

Ecology and Evolution

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“…These fitness benefits arise partly because parents can adjust their care in response to ecological challenges (e.g. temperature [6][7][8], predation risk [9,10]), which may buffer offspring by mitigating harsh early life conditions or by increasing offspring resilience to environmental stressors. This plasticity in parental care may therefore allow organisms to occupy harsher environments than they could have in the absence of this care [7].…”

Section: Introductionmentioning

confidence: 99%

Predator-induced transgenerational plasticity of parental care behaviour in male three-spined stickleback fish across two generations

Hellmann,

Keagy,

Carlson

et al. 2024

Proc. R. Soc. B.

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Parental care is a critical determinant of offspring fitness, and parents adjust their care in response to ecological challenges, including predation risk. The experiences of both mothers and fathers can influence phenotypes of future generations (transgenerational plasticity). If it is adaptive for parents to alter parental care in response to predation risk, then we expect F 1 and F 2 offspring who receive transgenerational cues of predation risk to shift their parental care behaviour if these ancestral cues reliably predict a similarly risky environment as their F 0 parents. Here, we used three-spined sticklebacks ( Gasterosteus aculeatus ) to understand how paternal exposure to predation risk prior to mating alters reproductive traits and parental care behaviour in unexposed F 1 sons and F 2 grandsons. Sons of predator-exposed fathers took more attempts to mate than sons of control fathers. F 1 sons and F 2 grandsons with two (maternal and paternal) predator-exposed grandfathers shifted their paternal care (fanning) behaviour in strikingly similar ways: they fanned less initially, but fanned more near egg hatching. This shift in fanning behaviour matches shifts observed in response to direct exposure to predation risk, suggesting a highly conserved response to pre-fertilization predator exposure that persists from the F 0 to the F 1 and F 2 generations.

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“…Warming has been shown to influence the distribution and behavior of many organisms (Abram et al, 2017;Freitas et al, 2021;Spatafora et al, 2021). Higher temperature may induce behavioral changes by altering activity rate (Biro et al, 2010), foraging (Biro et al, 2007;Hu et al, 2021), habitat use and selection (Freitas et al, 2016;Matis et al, 2018;Freitas et al, 2021), and reproduction (Hopkins et al, 2011;Miller et al, 2015;Spatafora et al, 2021). However, temperature-related changes in the organism's behavior may in turn affect species interactions and ecological processes (Harmon and Barton, 2013;Freitas et al, 2021;Zhang et al, 2022).…”

Section: Introductionmentioning

confidence: 99%

Different behavioral strategies of two sympatric seahorses: habitat availability and increased density of Hippocampus guttulatus alter the behavior of Hippocampus hippocampus

Spatafora,

Gristina,

Quattrocchi

et al. 2023

Front. Mar. Sci.

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In the light of future ocean warming scenarios and habitat fragmentation, coastal fishes must adjust their physiological and behavioral traits to face the combined effect of global warming and ecological interactions. Seahorses (Hippocampus spp.) are charismatic fishes with peculiar life cycle traits, which make them vulnerable to several anthropic pressures and natural disturbances. In this study, we investigated the behavior of two sympatric seahorse species, the long-snouted Hippocampus guttulatus (Cuvier, 1829) and the short-snouted Hippocampus hippocampus (Linnaeus, 1758). Specifically, we carried out two manipulative experiments to assess (i) the effect of temperature and habitat availability on both H. hippocampus and H. guttulatus behavior and (ii) the effect of temperature and an increased density of H. guttulatus (by 3×) on the activity level of congeneric species H. hippocampus. Our results showed that +3°C warming did not affect seahorse behavior in both experiments, suggesting greater behavioral tolerance to thermal variation. However, a significant reduction of the active behavior of H. hippocampus was observed when the artificial habitat was introduced in the tank, while H. guttulatus maintained its activity. Furthermore, a significant decrease of the H. hippocampus activity was observed with an increased relative dominance of H. guttulatus. Our results suggest that both increased density of H. guttulatus and habitat availability, but not ocean warming, will affect the behavior of H. hippocampus. Therefore, different interspecific behavioral strategies may occur, thus affecting the distribution of the two species among shallow habitats when they occur in sympatry.

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Plastic adjustments of biparental care behavior across embryonic development under elevated temperature in a marine ectotherm

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 3 publications

References 86 publications

Parents exposed to warming produce offspring lower in weight and condition

Parents exposed to warming produce offspring lower in weight and condition

Predator-induced transgenerational plasticity of parental care behaviour in male three-spined stickleback fish across two generations

Different behavioral strategies of two sympatric seahorses: habitat availability and increased density of Hippocampus guttulatus alter the behavior of Hippocampus hippocampus

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