Differential Tolerance and Seasonal Adaptation to Temperature and Salinity Stress at a Dynamic Range Boundary Between Estuarine Gastropods

Abstract

Insight into how coastal organisms will respond to changing temperature and salinity regimes may be derived from studies of adaptation to fluctuating estuarine environments, especially under stressful range-edge conditions. We characterized a dynamic range boundary between two estuarine sea slugs, Alderia modesta (distributed across the North Pacific and North Atlantic) and Alderia willowi, known from southern and central California. The species overlap from Bodega Bay to San Francisco Bay, where populations are dominated by A. modesta after winter rains but by A. willowi after peak summer temperatures. Laboratory assays confirmed superior tolerance to low salinity for the northern species, A. modesta: encapsulated embryos developed at 8 ppt, larvae survived at 4-6 ppt, and adults survived repeated exposure to 2 ppt, salinities that reduced development or survival for the same stages of A. willowi. Adults did not appreciably differ in their high-temperature threshold, however. Each species showed increased tolerance to either temperature or salinity stress at its range margin, indicating plasticity or local adaptation, but at the cost of reduced tolerance to the other stressor. At its northern limit, A. willowi became more tolerant of low salinity during the winter rainy season, but also less heat tolerant. Conversely, A. modesta became more heat resistant from spring to summer at its southern limit, but less tolerant of low salinity. Trade-offs in stress tolerance may generally constrain adaptation and limit biotic response to a rapidly changing environment, as well as differentiating species niches.

Plasticity and artificial selection for developmental mode in a poecilogonous sea slug

“…In this paper, I documented reduced survival in low salinity (possibly via environmentally induced inbreeding depression of self-fertilized egg masses, see Cheptou & Donohue, 2011). Low salinity leads to significantly longer developmental times and significantly reduced hatching success of both lecithotrophic and planktotrophic A. willowi larvae (Krug et al, 2021).…”

“…Egg‐mass type plasticity only occurs once in the Alderia genus, for which planktotrophy is the ancestral state and the only other mode of development (i.e., there are no lecithotrophic Alderia species, Krug et al., 2015 ). In A. willowi , it appears plasticity for egg‐mass type has evolved alongside adaptations to the higher ambient temperature and less frequent low‐salinity events of their Central and Southern California habitats (Krug et al., 2012 , 2021 ). Salinity is a common stressor for estuarine animals that varies seasonally in California (Cloern et al., 2017 ).…”

“…In this paper, I documented reduced survival in low salinity (possibly via environmentally induced inbreeding depression of self‐fertilized egg masses, see Cheptou & Donohue, 2011 ). Low salinity leads to significantly longer developmental times and significantly reduced hatching success of both lecithotrophic and planktotrophic A. willowi larvae (Krug et al., 2021 ). Planktotrophic larvae typically hatch from the encapsulated egg mass earlier than lecithotrophic larvae (Krug, 1998 ) and even under low‐salinity stress (12 ppt) planktotrophic A. willowi larvae hatch earlier than lecithotrophic larvae (Krug et al., 2021 ), possibly reducing their time spent in stressful low‐salinity near‐shore conditions.…”

“…and Southern California habitats (Krug et al, 2012(Krug et al, , 2021. Salinity is a common stressor for estuarine animals that varies seasonally in California (Cloern et al, 2017).…”

“…Planktotrophic larvae typically hatch from the encapsulated egg mass earlier than lecithotrophic larvae (Krug, 1998) and even under low-salinity stress (12 ppt) planktotrophic A. willowi larvae hatch earlier than lecithotrophic larvae (Krug et al, 2021), possibly reducing their time spent in stressful low-salinity near-shore conditions.…”