Warming of the oceans due to climate change continues to threaten marine biodiversity, including keystone species with cultural and economic importance. Genetic diversity will play a crucial role in the adaptation of species, but how do genetic diversity and ontogeny act together to shape the thermal resilience of a species? In New Zealand seawater temperatures are increasing by 0.1-0.3oC per decade (Shears & Bowen, 2017; Sutton & Bowen, 2019), and as global air and seawater temperatures are projected to increase further in the future (IPCC, 2022) this is putting pressure on marine species and communities. A clear image of how fast seawater temperatures are changing is shown in Figure 1. Here, a side-by-side comparison of the maximum sea surface temperature (SST) is shown, with the left panel (A) representing the whole last two decades (2003-2023), while the right panel (B) includes the SST recorded for January 2024, where a heatwave event took place in New Zealand that far exceeded any maximum observed over the last 20 years. These steady increases in seawater temperature and the rapid increases due to heatwave events are a major threat to marine species.
The green-lipped mussel (Perna canaliculus), also known by indigenous Māori as kuku or kūtai, is an iconic species in New Zealand, not only for its cultural importance but also because this mussel species is one of the most important aquaculture crops in the country - known by its trademark name, GreenshellTM mussel (GSM).
GreenshellTM mussels have been selectively bred in New Zealand for more than two decades with the objective of obtaining better meat yield, and fast-growing mussels (Camara & Symonds, 2014). However, in recent years, there has been an interest in selecting for other traits such as thermal tolerance, in order to future-proof the production of the species (Ericson et al., 2023). The selective breeding programme also allows scientists to work with a globally unique biological resource.
Thermal tolerance, defined by how a species responds to thermal stress is species-specific and can change through life, with different life stages having different thermal resilience. Therefore, for the work presented in the article published in Scientific Reports (Delorme et al., 2024), we wanted to evaluate how thermal tolerance in GreenshellTM mussels is influenced by genetics and also age. Figure 2 shows a summary of the experimental design. We used six genetically distinct bi-parental families and tested them at four different ages, ranging from mussels that were 6 weeks old to 1-year-old mussels. We exposed the mussels to acute heat challenges to determine their median lethal temperature (LT50) as an indicator of thermal tolerance, and complemented the whole-animal response with measurement of a well-established molecular marker - gene expression of the 70kDa heat shock protein - hsp70.
The complete experiment was labour-intensive and included the assessment of just over 57,000 mussels in total. A large team of researchers and technicians helped with the project, from cultivating microalgae to feed the mussels, maintaining the seawater systems, running the experiments, assessing mussel survival under the microscope (Figure 3), analysing samples in the molecular laboratory and running the statistical analyses. Results showed that ontogeny influences thermal tolerance in Perna canaliculus, with early juveniles showing greater heat tolerance compared to sub-adult mussels. At the same time, genetics also plays a fundamental role in the ability of the mussels to tolerate higher temperatures. Interestingly, individual mussel size also had an important role in determining the tolerance of mussels to thermal stress within each age, with the larger mussels from each family (even the most resilient families) showing a tendency to be more vulnerable to temperature (See Figure 3). One-year-old mussels responded to the acute heat challenge by upregulating the hsp70 gene, with upregulation levels correlating with thermal tolerance (LT50) and net family survival.
Investigating the response of marine organisms to higher temperatures is critical to understand coping mechanisms and potential for adaptation to climate change. The fact that some mussel families showed higher thermal tolerances (LT50) suggests that those families are physiologically better adapted to cope with challenging conditions, having also direct importance for the aquaculture industry for selective breeding purposes. Selective breeding of thermotolerant mussels could be applied to future-proof the species, with due attention given to the age at which family-level selection is applied.
Finally, the authors would like to acknowledge the funding provided by the New Zealand Ministry of Business, Innovation and Employment (MBIE) under the Cawthron Shellfish Aquaculture Research Platform (ShARP). We would also like to thank the mussel hatchery SPATnz and BreedCo for providing the mussels for experimentation, and to everyone who supported this research.
References
Camara, M. D., & Symonds, J. E. (2014). Genetic improvement of New Zealand aquaculture species: programmes, progress and prospects. New Zealand Journal of Marine and Freshwater Research, 48(3), 466-491. https://doi.org/10.1080/00288330.2014.932291
Delorme, N. J., King, N., Cervantes-Loreto, A., South, P. M., Baettig, C. G., Zamora, L. N., Knight, B. R., Ericson, J. A., Smith, K. F., & Ragg, N. L. C. (2024). Genetics and ontogeny are key factors influencing thermal resilience in a culturally and economically important bivalve. Scientific Reports, 14(1), 19130. https://doi.org/10.1038/s41598-024-70034-0
Ericson, J. A., Laroche, O., Biessy, L., Delorme, N. J., Pochon, X., Thomson-Laing, J., Ragg, N. L. C., & Smith, K. (2023). Differential responses of selectively bred mussels (Perna canaliculus) to heat stress -survival, immunology, gene expression and microbiome diversity. Frontiers in Physiology, 14. https://doi.org/10.3389/fphys.2023.1265879
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