Variation in Thermal Tolerance of the Giant Kelp’s Gametophytes: Suitability of Habitat, Population Quality or Local Adaptation?

Abstract

The giant kelp Macrocystis pyrifera is a cosmopolitan species of cold-temperate coasts. Its South-American distribution ranges from Peru to Cape Horn and Argentina, encompassing a considerable temperature gradient, from 3 to 20°C. Temperature is known to strongly affect survival, growth and reproduction of many kelp species, and ongoing global warming is already eroding their range distribution. Their response to thermal variability was shown to vary among genetically differentiated regions and populations, suggesting a possible adaptive divergence in thermal tolerance traits. This study aimed at testing the existence of local adaptation in the giant kelp, in regions separated by up to 4000km and strong thermal divergence. Two complementary experiments mimicked reciprocal transplants through a common garden approach, each habitat being represented by a given temperature corresponding to the regional average of the sampled populations. Several proxies of fitness were measured in the haploid stage of the kelp, and sympatric versus allopatric conditions (i.e. individuals at the temperature of their region of origin versus in a different temperature and versus individuals from other regions in that temperature) were compared. Additionally, a heat wave at 24°C was applied to measure the tolerance limits of these gametophytes. A significant interaction between experimental temperature and region of origin revealed that temperature tolerance varied among regions. However, depending on the fitness parameter measured, high latitude populations from the sub-Antarctic region were not always less heat resilient than populations from the warmer region of Peru. Even at 24°C, a temperature that is exceptionally reached in the southernmost part of the kelp’s natural habitat, all the gametophytes survived, although with strong differences in other traits among regions and populations within regions. This large range of temperature tolerance supports the idea of kelp gametophytes being a resistant stage. Finally, local adaptation sensu stricto was not detected. Fertility was more influenced by the geographic origin than by temperature, with possible effects of marginal conditions at the extremes of the distribution range. The latter results also suggest that stochastic dynamics such as genetic drift restricts adaptive processes in some populations of M. pyrifera.

Microscopic Stages of North Atlantic Laminaria digitata (Phaeophyceae) Exhibit Trait-Dependent Thermal Adaptation Along Latitudes

“…Although none of the populations are likely to experience such high SSTs over 14 days in their natural environment, it should be noted that our experimental priming temperature of 24°C only exceeds the mean summer SST at the southern-most location in Quiberon by ~6°C, but by 18-19°C at the northern-most limit of the species in Spitsbergen (Oppliger et al, 2014;Fischer et al, 2019). Few studies have examined the intra-specific thermal response of microscopic gametophyte and sporophyte stages throughout their distribution gradient (Martinez, 1999;Oppliger et al, 2012;Mohring et al, 2014;Becheler et al, 2022). However, several previous studies have shown that the upper lethal limit with respect to survival and growth of gametophytes of Atlantic Laminaria spp.…”

“…Even though projected shifts in distribution patterns frequently presume that individuals of a species respond uniformly to climate change, there is evidence for intraspecific variation among populations of kelps (King et al, 2018;King et al, 2019;Liesner et al, 2020a;Becheler et al, 2022). In S. latissima, local mortality thresholds of sporophytes differ by ~3°C between populations from the NE and NW Atlantic, so single temperature tolerances should not be assumed to apply over an entire species' distribution (Filbee-Dexter et al, 2020).…”

“…Populations at the warm range edge are expected to contain unique genetic diversity that was maintained across glacial cycles (Maggs et al, 2008;Assis et al, 2017a), which may provide them with high physiological versatility and resilience (Wernberg et al, 2018), but these are especially threatened in the face of climate change. Furthermore, species with broad spatial distributions, occupying a range of thermal niches, may also have evolved unique genetic and phenotypic characteristics (Martins et al, 2020;Becheler et al, 2022). One of the best methods to study adaptive changes along latitudinal gradients are common-garden experiments (King et al, 2018;Martins et al, 2020;Becheler et al, 2022), in which material from different populations is subjected to the same environment, regardless of the geographical and environmental origin of populations.…”

“…Furthermore, species with broad spatial distributions, occupying a range of thermal niches, may also have evolved unique genetic and phenotypic characteristics (Martins et al, 2020;Becheler et al, 2022). One of the best methods to study adaptive changes along latitudinal gradients are common-garden experiments (King et al, 2018;Martins et al, 2020;Becheler et al, 2022), in which material from different populations is subjected to the same environment, regardless of the geographical and environmental origin of populations. However, rather than dealing with multiple parental strains to yield substantial genetic representation, past studies have primarily used single clonal strains, but this has changed lately (e.g., Liesner et al, 2020a;Liesner et al, 2020b;Becheler et al, 2022;Gauci et al, 2022).…”

Season influences interspecific responses of canopy‐forming kelps to future warming and acidification at high latitude

“…Sitka Sound is situated at the poleward edge of M. pyrifera 's continuous range extent (Druehl, 1970, 1981). Although intrapopulation variation in thermal tolerance has been observed in this species (Hollarsmith et al, 2020), these northern fringing M. pyrifera populations may possess enough phenotypic plasticity to afford a relative tolerance to anticipated OW conditions in this region (Becheler et al, 2022; King et al, 2020).…”