Plasticity of fertilization rates under varying temperature in the broadcast spawning mussel,Mytilus galloprovincialis

Abstract

Oceans are a huge sink for the increased heat associated with anthropogenic climate change, and it is vital to understand the heat tolerance of marine organisms at all life stages to accurately predict species’ responses. In broadcast spawning marine invertebrates, reproduction is a vulnerable process in which sperm and eggs are released directly into the open water. Gametes are then exposed to fluctuating environmental conditions that may impact their fertilizing capacity. Using the broadcast spawning Mediterranean mussel, Mytilus galloprovincialis, as a model species, we performed blocks of factorial mating crosses to assess the variance in fertilization rates among individuals under both ambient and elevated temperatures. Overall, we found a small, but significant decline in fertilization rates with elevated temperatures. However, there was substantial plasticity in responses, with particular mussels having increased fertilization under elevated temperatures, although the majority showed decreased fertilization rates. Our results suggest possible future reproductive costs to ocean warming in M. galloprovincialis, although it is also possible that genetic variation for thermal sensitivity may allow for adaptation to changing environmental conditions.

RNA-seq coupled to proteomic analysis reveals high sperm proteome variation between two closely related marine mussel species

“…There is evidence that changes in seawater temperature may affect sperm function. Thus in M. galloprovincialis higher temperature is associated with lower fertilization rates on average [164] and sperm motility and linearity of swimming patterns are affected by temperature and its interaction with pH [165]. This may have fitness consequences as swimming speed has also been associated with higher fertilisation rates [166].…”

Post-ejaculation thermal stress causes changes to the RNA profile of sperm in an external fertilizer

“…Australian populations of M. galloprovincialis, which contain signatures of both a native southern lineage and more recently introduced northern individuals [30][31][32], are distributed across the southern coastline where they experience relatively high rates of sea surface warming, and have also been subject to several prolonged heatwave events in recent years where nearshore sea surface temperatures of up to 6°C above average have consistently been recorded [8,10]. Such temperature anomalies can have substantial effects on fitness across various life stages in M. galloprovincialis, including fertilization success, larval viability and adult mortality [33][34][35]. These factors, as well as the tractability of M. galloprovincialis for spawning and gamete manipulation experiments (e.g.…”

Exploring impacts of marine heatwaves: paternal heat exposure diminishes fertilization success in the purple sea urchin (Strongylocentrotus purpuratus)

“…This species-dependent thermal tolerance of fertilization is observed across other marine invertebrate taxa as well, including corals (Negri et al 2007;Albright and Mason 2013) and mollusks (Parker et al 2010;Armstrong et al 2019;Enricuso et al 2019). There is also evidence that a great deal of intra-species variability in fertilization success exists, with contrasting results observed in the mussel, Mytilus edilus (Eads et al 2016a(Eads et al , 2016b, the sea urchin, Heliocidaris erthyogramma (Byrne et al 2009(Byrne et al , 2010a(Byrne et al , 2010b, and the polychaete, Galeolaria caespitosa (Kupriyanova and Havenhand 2005;Chirgwin et al 2020). This variation highlights the need to consider other factors, both biological (e.g.…”

“…Methodological differences in fertilization success assays are common across studies, an issue prompting the creation of a more standardized approach for environmental monitoring (Lera et al 2006). The type of crossing design used, for example, can heavily influence results, with the use of pooled gametes reducing the effects of male-female incompatibilities (Byrne et al 2009;Eads et al 2016b) and benefitting from the positive contributions of polyandry (Evans and Marshall 2005), while individual male-female pairings instead illuminate the extent of intra-individual variability within fertilization (Foo et al 2014;Eads et al 2016a). Our study employed the less-frequently used split-clutch design where sperm from individual males were used to fertilize eggs from the same pool of females (Crean et al 2013).…”

“…Fertilization can occur with unaltered success under moderate increases in temperature for many species (Byrne et al 2010a;Enricuso et al 2019;Pitts et al 2020), with several studies observing positive effects of elevated temperature on echinoderm and mollusk fertilization (Ho et al 2013;Foo et al 2014;Eads et al 2016b). Alternatively, a handful of studies document decreased fertility under high temperature (Parker et al 2010;Albright and Mason 2013), with these conflicting results even observed within the same species challenged by similar temperatures (Byrne et al 2009;Eads et al 2016a;Chirgwin et al 2020). These inconsistencies highlight the variability associated with measuring fertilization success as a result of differences in methods, parental crossing designs, distances between experimental temperatures from the study organism's thermal limits, and parental environmental histories (Byrne 2011).…”