Using clones and copper to resolve the genetic architecture of metal tolerance in a marine invader

Abstract

The global spread of invasive species may be facilitated by adaptation to the practices that humans use to manage those species. For example, marine invertebrates that adapt to metal-based antifouling biocides on ship hulls may be more likely to be introduced to and establish in metal-polluted environments. We tested this idea by studying clonal variation in tolerance to, and ability to recover from, exposure to copper in a widespread invasive marine bryozoan, Watersipora subtorquata. We cloned colonies of this organism to independently test multiple environments in a genotype by environment design, and then created a genetic variance–covariance matrix. Genotypes were exposed to a gradient of copper concentrations and growth measured during exposure and after a recovery period. There was a significant genotype × environment interaction in growth during exposure and recovery. We found clonal variation in tolerance and ability to recover from exposure to copper, with growth during exposure apparently trading off against growth after exposure. A weak genetic correlation between growth during and after exposure further indicated that they are separate traits. Overall, the genetic variation within this population indicates that there is considerable potential for adaptation to copper, but this comes at a cost to growth in unpolluted environments.

Family‐level variation in early life‐cycle traits of kelp

“…, McKenzie et al. ). Furthermore, the overall average of each family‐level trait value was close to that of the mixed families mean trait values, providing further evidence that the first generation fitness costs of inbreeding in animals and plants are not apparent in kelps (Barner et al.…”

“…However, as it was only possible to determine broad sense heritability these ADAPTIVE POTENTIAL OF KELP estimates include both additive and non-additive genetic effects in addition to possible maternal effects. Although broad sense heritability has its limitations, there are numerous studies of marine organisms for which sire and dam effects cannot be partitioned, or which are restricted by clonal or inbreeding designs, where it provides a basis for interpreting adaptation (Wright et al 2004, Cs asz ar et al 2010, McKenzie et al 2012). Furthermore, the overall average of each family-level trait value was close to that of the mixed families mean trait values, providing further evidence that the first generation fitness costs of inbreeding in animals and plants are not apparent in kelps (Barner et al 2011), likely due to genetic recombination (meiosis) during spore production and purging of deleterious alleles in the haploid stage.…”

“…Many of these tests rely on estimates of broad-sense heritability (Cs asz ar et al 2010) which provides an upper estimate of heritability due to potential inheritance of non-genetic components. In addition to understanding trait heritability, the relative performance of genotypes across multiple environments (Bowman 1972; via genotype 9 environment studies) is a means of exploring the adaptive response of quantitative traits (e.g., describing phenology, morphology, and physiology; Galletly et al 2007, Hawkins et al 2010, Pease et al 2010, McKenzie et al 2012 to environmental stressors.…”

Adaptation in marine invasion: a genetic perspective

“…While this evidence is suggestive, without multi-generational common garden rearing it is impossible to definitively attribute these differences to genetic adaptation as opposed to plasticity. Other quantitative studies take advantage of the clonal nature of many fouling organisms to examine variation between individuals in an implicitly genetic context, providing clearer evidence of molecular evolution (McKenzie et al 2011(McKenzie et al , 2012.…”

“…However, there is a growing body of work suggesting that invasive fouling species may be evolving copper tolerance in response (Piola et al 2009), which may lend them a competitive advantage over native fouling species (Crooks et al 2010). Evidence for copper tolerance adaptation in invasive fouling species comes from two bryozoans, B. neritina and Watersipora subtorquata, and the tunicate Styela plicata (Piola and Johnston 2006;Galletly et al 2007;McKenzie et al 2011McKenzie et al , 2012. Outside of the fouling community, different performance in high-pollution conditions has been recorded for high-and low-pollution populations of the barnacle Amphibalanus amphitrite, the clam Venerupis philippinarum, and the snail L. saxatilis (Daka and Hawkins 2004;Paul-Pont et al 2010;Romano et al 2010).…”