Rising atmospheric CO 2 reduces seawater pH causing ocean acidification (OA). Understanding how resilient marine organisms respond to OA may help predict how community dynamics will shift as CO 2 continues rising. The common slipper shell snail Crepidula fornicata is a marine gastropod native to eastern North America that has been a successful invader along the western European coastline and elsewhere. It has also been previously shown to be resilient to global change stressors. To examine the mechanisms underlying C. fornicata’s resilience to OA, we conducted two controlled laboratory experiments. First, we examined several phenotypes and genome-wide gene expression of C. fornicata in response to pH treatments (7.5, 7.6, and 8.0) throughout the larval stage and then tested how conditions experienced as larvae influenced juvenile stages (i.e., carry-over effects). Second, we examined genome-wide gene expression patterns of C. fornicata larvae in response to acute (4, 10, 24, and 48 h) pH treatment (7.5 and 8.0). Both C. fornicata larvae and juveniles exhibited resilience to OA and their gene expression responses highlight the role of transcriptome plasticity in this resilience. Larvae did not exhibit reduced growth under OA until they were at least 8 days old. These phenotypic effects were preceded by broad transcriptomic changes, which likely served as an acclimation mechanism for combating reduced pH conditions frequently experienced in littoral zones. Larvae reared in reduced pH conditions also took longer to become competent to metamorphose. In addition, while juvenile sizes at metamorphosis reflected larval rearing pH conditions, no carry-over effects on juvenile growth rates were observed. Transcriptomic analyses suggest increased metabolism under OA, which may indicate compensation in reduced pH environments. Transcriptomic analyses through time suggest that these energetic burdens experienced under OA eventually dissipate, allowing C. fornicata to reduce metabolic demands and acclimate to reduced pH. Carry-over effects from larval OA conditions were observed in juveniles; however, these effects were larger for more severe OA conditions and larvae reared in those conditions also demonstrated less transcriptome elasticity. This study highlights the importance of assessing the effects of OA across life history stages and demonstrates how transcriptomic plasticity may allow highly resilient organisms, like C. fornicata , to acclimate to reduced pH environments.
more »
« less
Gene expression patterns of red sea urchins (Mesocentrotus franciscanus) exposed to different combinations of temperature and pCO2 during early development
Abstract Background The red sea urchin Mesocentrotus franciscanus is an ecologically important kelp forest herbivore and an economically valuable wild fishery species. To examine how M. franciscanus responds to its environment on a molecular level, differences in gene expression patterns were observed in embryos raised under combinations of two temperatures (13 °C or 17 °C) and two p CO 2 levels (475 μatm or 1050 μatm). These combinations mimic various present-day conditions measured during and between upwelling events in the highly dynamic California Current System with the exception of the 17 °C and 1050 μatm combination, which does not currently occur. However, as ocean warming and acidification continues, warmer temperatures and higher p CO 2 conditions are expected to increase in frequency and to occur simultaneously. The transcriptomic responses of the embryos were assessed at two developmental stages (gastrula and prism) in light of previously described plasticity in body size and thermotolerance under these temperature and p CO 2 treatments. Results Although transcriptomic patterns primarily varied by developmental stage, there were pronounced differences in gene expression as a result of the treatment conditions. Temperature and p CO 2 treatments led to the differential expression of genes related to the cellular stress response, transmembrane transport, metabolic processes, and the regulation of gene expression. At each developmental stage, temperature contributed significantly to the observed variance in gene expression, which was also correlated to the phenotypic attributes of the embryos. On the other hand, the transcriptomic response to p CO 2 was relatively muted, particularly at the prism stage. Conclusions M. franciscanus exhibited transcriptomic plasticity under different temperatures, indicating their capacity for a molecular-level response that may facilitate red sea urchins facing ocean warming as climate change continues. In contrast, the lack of a robust transcriptomic response, in combination with observations of decreased body size, under elevated p CO 2 levels suggest that this species may be negatively affected by ocean acidification. High present-day p CO 2 conditions that occur due to coastal upwelling may already be influencing populations of M. franciscanus .
more »
« less
- Award ID(s):
- 1831937
- NSF-PAR ID:
- 10378029
- Date Published:
- Journal Name:
- BMC Genomics
- Volume:
- 22
- Issue:
- 1
- ISSN:
- 1471-2164
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Phenotypic plasticity and adaptive evolution enable population persistence in response to global change. However, there are few experiments that test how these processes interact within and across generations, especially in marine species with broad distributions experiencing spatially and temporally variable temperature and p CO 2 . We employed a quantitative genetics experiment with the purple sea urchin, Strongylocentrotus purpuratus , to decompose family-level variation in transgenerational and developmental plastic responses to ecologically relevant temperature and p CO 2 . Adults were conditioned to controlled non-upwelling (high temperature, low p CO 2 ) or upwelling (low temperature, high p CO 2 ) conditions. Embryos were reared in either the same conditions as their parents or the crossed environment, and morphological aspects of larval body size were quantified. We find evidence of family-level phenotypic plasticity in response to different developmental environments. Among developmental environments, there was substantial additive genetic variance for one body size metric when larvae developed under upwelling conditions, although this differed based on parental environment. Furthermore, cross-environment correlations indicate significant variance for genotype-by-environment interactive effects. Therefore, genetic variation for plasticity is evident in early stages of S. purpuratus , emphasizing the importance of adaptive evolution and phenotypic plasticity in organismal responses to global change.more » « less
-
more » « less
Abstract Understanding genome‐wide responses to environmental conditions during embryogenesis is essential for discerning the evolution of developmental plasticity and canalization, two processes generating phenotypic variation targeted by natural selection. Here, we present the first comparative trajectory analysis of matched transcriptomic developmental time series from two reptiles incubated under identical conditions, a turtle with a ZZ/ZW system of genotypic sex determination (GSD),
Apalone spinifera , and a turtle with temperature‐dependent sex determination (TSD),Chrysemys picta . Results from our genome‐wide, hypervariate gene expression analysis of sexed embryos across five developmental stages revealed that substantial transcriptional plasticity in the developing gonads can persist for >145 Myr, long after the canalization of sex determination via the evolution of sex chromosomes, while some gene‐specific thermal sensitivity drifts or evolves anew. Such standing thermosensitivity represents an underappreciated evolutionary potential harbored by GSD species that may be co‐opted during future adaptive shifts in developmental programing, such as a GSD to TSD reversal, if favored by ecological conditions. Additionally, we identified novel candidate regulators of vertebrate sexual development in GSD reptiles, including sex‐determining candidate genes in a ZZ/ZW turtle. -
more » « less
Abstract The deep ocean releases large amounts of old, pre‐industrial carbon dioxide (CO2) to the atmosphere through upwelling in the Southern Ocean, which counters the marine carbon uptake occurring elsewhere. This Southern Ocean CO2release is relevant to the global climate because its changes could alter atmospheric CO2levels on long time scales, and also affects the present‐day potential of the Southern Ocean to take up anthropogenic CO2. Here, year‐round profiling float measurements show that this CO2release arises from a zonal band of upwelling waters between the Subantarctic Front and wintertime sea‐ice edge. This band of high CO2subsurface water coincides with the outcropping of the 27.8 kg m−3isoneutral density surface that characterizes Indo‐Pacific Deep Water (IPDW). It has a potential partial pressure of CO2exceeding current atmospheric CO2levels (∆PCO2) by 175 ± 32 μatm. Ship‐based measurements reveal that IPDW exhibits a distinct ∆PCO2maximum in the ocean, which is set by remineralization of organic carbon and originates from the northern Pacific and Indian Ocean basins. Below this IPDW layer, the carbon content increases downwards, whereas ∆PCO2decreases. Most of this vertical ∆PCO2decline results from decreasing temperatures and increasing alkalinity due to an increased fraction of calcium carbonate dissolution. These two factors limit the CO2outgassing from the high‐carbon content deep waters on more southerly surface outcrops. Our results imply that the response of Southern Ocean CO2fluxes to possible future changes in upwelling are sensitive to the subsurface carbon chemistry set by the vertical remineralization and dissolution profiles.
-
more » « less
Abstract Ocean acidification (OA) from seawater uptake of rising carbon dioxide emissions impairs development in marine invertebrates, particularly in calcifying species. Plasticity in gene expression is thought to mediate many of these physiological effects, but how these responses change across life history stages remains unclear. The abbreviated lecithotrophic development of the sea urchin
Heliocidaris erythrogramma provides a valuable opportunity to analyse gene expression responses across a wide range of life history stages, including the benthic, post‐metamorphic juvenile. We measured the transcriptional response to OA inH. erythrogramma at three stages of the life cycle (embryo, larva, and juvenile) in a controlled breeding design. The results reveal a broad range of strikingly stage‐specific impacts of OA on transcription, including changes in the number and identity of affected genes; the magnitude, sign, and variance of their expression response; and the developmental trajectory of expression. The impact of OA on transcription was notably modest in relation to gene expression changes during unperturbed development and much smaller than genetic contributions from parentage. The latter result suggests that natural populations may provide an extensive genetic reservoir of resilience to OA. Taken together, these results highlight the complexity of the molecular response to OA, its substantial life history stage specificity, and the importance of contextualizing the transcriptional response to pH stress in light of normal development and standing genetic variation to better understand the capacity for marine invertebrates to adapt to OA.
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1186/s12864-020-07327-x
