Estimating the heritable genetic variation in fitness-related traits is key to projecting the adaptive evolution of organisms in response to a changing environment. While heritability studies on reef-building corals to date support adaptive capacity, little is known about the dynamics of trait heritability across life stages in which distinct selective pressures can have long-lasting effects both within and across generations. In this study, we obtained heritability estimates for energetic and thermal stress response traits in larval, recruit, and adult Porites astreoides from two populations in the Lower Florida Keys. To induce bleaching phenotypes among individual families, larvae were exposed to a 4-day thermal stress at 32 ˚C, whereas adults and recruits received the same treatment for 22 days. Origin-dependent tolerance was observed in two life stages where offshore recruits lost more symbiont cells under heat than inshore recruits compared to their respective controls and heat-treated offshore adults suffered a greater loss in total protein content. Surprisingly, larvae appeared to be largely insensitive to heat regardless of origin. Broad sense heritability (H 2 ) estimates varied greatly among traits and life stages, which may reflect changes in the relative importance of genetic and environmental variation throughout development. Notably, more than 80% of the variation in larval chlorophyll a concentration was attributed to genetic factors. The overall moderate to high H 2 estimates measured here suggest these corals have considerable potential to adapt to environmental change.
Amongst the most prominent driving factors behind this were the invasion of the Great Lakes by the zebra mussel Dreissena polymorpha Pallas, 1771 in the 1980s and reports of an average of one new species invading San Francisco Bay every 14 weeks between 1961 to 1995 (Cohen and Carlton 1998). At this time, scientists were becoming well aware of the growing number of introductions worldwide and their impacts on marine communities (Minchin 1996; Reise et al. 1998; Hewitt et al. 1999; Sliwa et al. 2009). Ascidians, commonly known as sea squirts, were quickly flagged as one of the most notorious and diverse group of fouling species being transported and introduced around the world (Shenkar and Swalla 2011). Indeed, in the late 1990s and early 2000s, invasive ascidians were identified as important players causing significant ecological and economic impacts to marine systems (Coles et al. 2002; Lambert 2002). As the twenty-first century enters its third decade, invasive ascidians continue to affect ecosystems (Carman et al. 2011; Shenkar 2012; Zhan et al. 2015), create problems for aquaculture (Muñoz and McDonald 2014; McKenzie et al. 2017), and frequently dominate coastal fouling communities (López-Legentil et al. 2015). The International Invasive Sea Squirt Conference (IISSC; https://web. whoi.edu/sea-squirt-conference/) began in 2005 to bring together diverse user groups concerned about invasive ascidians. The goal was to explore invasive ascidian biology, ecology, impacts and management options. The conference audience included marine biologists, shellfishery scientists and industry, governmental agencies concerned with coastal resources, representatives from sponsoring organizations and the media. The first IISSC was so successful that it became more or less a biennial event, with
The ability for adaptation to track environmental change depends on how efficiently selection can act on heritable genetic variation. Complex life cycles may promote or constrain adaptation depending on the integration or independence of fitness-related traits over development. Reef-building corals exhibit life cycle complexity and are sensitive to increasing temperatures, highlighting the need to understand heritable potential of the thermal stress response and its developmental regulation. We used tag-based RNA-seq to profile holobiont gene expression of inshore and offshore Porites astreoides adults and recruit offspring in response to a 16-day heat stress, and larvae in response to a 4-day heat stress. Host developmental stage affected both broad patterns of host and symbiont expression, and modulated the stress response in both partners, suggesting that symbiotic interactions could vary between host developmental stages and influence the thermal stress response. Populations also exhibited origin-specific treatment responses, but response magnitude differed among life-stages. Inshore parents and recruit offspring exhibited a more robust stress response, exhibiting greater expression profile divergence and differentially expressing more genes compared to offshore-origin corals. This suggests genetic or epigenetic inheritance of regulatory mechanisms giving rise to expression plasticity, although ontogenetic plasticity as a result of the local reef environment during larval development could also explain the origin effect. However, larval populations exhibited the opposite response, with offshore larvae exhibiting a more robust stress response, possibly due to stage-specific effects or exposure duration. Overall, these results show that putatively adaptive regulatory variation persists in thermally naïve life stages, but thermally responsive genes are stage-specific, which could complicate the evolutionary response of corals to climate change.
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