Evidence of selection for resistance to paralytic shellfish toxins during the early life history of soft‐shell clam, Mya arenaria, populations

Abstract

This study identifies early, postmetamorphic soft-shell clams, Mya arenaria, as the life-history stage most susceptible to effects of blooms of paralytic shellfish poisoning (PSP) toxin-producing Alexandrium spp. Laboratory experiments used progeny from predominantly susceptible (naïve) or resistant (annually exposed) NW Atlantic populations. Growth and survival of toxified veliger larvae did not differ from those fed nontoxic algae. In contrast, postlarvae (4-12-mm shell length) from both populations exposed to a highly toxic Alexandrium tamarense isolate (, 100 cells mL 21 , 64-69 pg saxitoxin equivalents [STXeq] cell 21 ) suffered burrowing incapacitation, toxin accumulation, and mortalities within 1 week of toxin exposure. These effects were greater and occurred sooner in the naïve population. Short-term toxification in the laboratory caused a significant shift in the genotypic composition of this population, determined with a molecular marker for sodium-channel resistance. Clams with the sensitive genotype were selectively eliminated relative to resistant or heterozygote clams. Ingestion of toxic cells (too large for larval capture) is thus required to elicit toxic effects. Exposure to mixed, toxic, and nontoxic algal suspensions demonstrated that adverse effects to fitness (survival and growth) were dose-dependent, occurring only at $ 50 cells mL 21 of the isolate used (PR18b). Paralysis and thus increased predatory risk occurred even at 10 cells mL 21 . Postlarvae , 12 mm, which can co-occur with red tides throughout the Atlantic range of M. arenaria, were more susceptible to PSP than large (. 30 mm) juveniles. Natural selection for resistance in Atlantic populations will thus vary latitudinally with the timing, duration, and intensity of toxic blooms.

Effects of toxic Alexandrium tamarense on behavior, hemocyte responses and development of brown ring disease in Manila clams

“…This agrees with prior findings that mortalities of subadult Mya arenaria (33 to 47 mm SL) typically started only after ~1 to 2 wk of exposure to 100 cells ml -1 of the same isolate (MacQuarrie & Bricelj 2008). Greater vulnerability to PSTs of small clams was also demonstrated when burrowing and survival were compared between Mya arenaria~12 mm and 35 mm SL exposed to comparable toxin concentrations (Bricelj et al 2010). Burrowing capacity is a critically important fitness parameter that is likely under strong natural selection, especially in juvenile bivalves before they attain a size refuge from predators.…”

“…1). The Alexandrium tamarense exposure concentration was selected based on prior experiments with juvenile (4 mm) Mya arenaria, in which 100 cells ml -1 caused severe mortalities, 10 cells ml -1 had no effect on survival or growth, although it affected motility, and 50 cells ml -1 caused 15% mortalities by the end of 2 wk and severe growth inhibition (Bricelj et al 2010). Cell densities of A. tamarense in the experimental tanks were determined microscopically and those of Isochrysis galbana were determined with an electronic Coulter counter.…”

“…Exposure to toxic Alexandrium spp. thus causes paralysis of the foot and pallial musculature in sensitive Mya arenaria, leading to burrowing incapacitation (MacQuarrie & Bricelj 2008, Bricelj et al 2010, which may increase predatory risk in nature. In this bivalve species, pronounced individual differences in the capacity to accumulate PSTs and in the resistance to the effects of these neurotoxins have been attributed to a single point mutation that encodes for a single amino acid substitution in Domain II of the pore region of the Na + channel protein (Bricelj et al 2005).…”

A novel mutation from gene splicing of a voltage-gated sodium channel in a marine copepod and its potential effect on channel function

“…The mutation allows nerve transmission to occur normally in resistant animals even under toxic food conditions (Bricelj et al, 2005); resistant clams outcompete susceptible individuals and predominate in areas where toxic Alexandrium spp. occur (Bricelj et al, 2010;Connell et al, 2007). Similar mutations confer resistance to tetrodotoxin, a toxin that also blocks sodium channels, in snakes (Geffeney et al, 2002) and pufferfish (Venkatesh et al, 2005).…”

Assessment of sodium channel mutations in Makah tribal members of the U.S. Pacific Northwest as a potential mechanism of resistance to paralytic shellfish poisoning

“…Twarog (1974) also theorized that recurrently exposed shellfish populations may undergo a genetic adaptation to PSTs with natural selection against individuals sensitive to the toxins. Research on the soft-shelled clam ( Mya arenaria ) has shown an adaptation in clam populations from geographical regions with prior history of exposure to PSTs where the substitution of a single amino acid can confer resistance to STX (Bricelj et al, 2005; Connell et al, 2007; MacQuarrie and Bricelj, 2008; Bricelj et al, 2010). The specific substitution elucidated in in M. arenaria was a simple change from adenine (A) to cytosine (C) in the domain II pore region of the alpha-subunit of the voltage-gated Na + channel (Bricelj et al, 2005).…”