Ecosystem size shapes antipredator trait evolution in estuarine threespine stickleback

Abstract

Ecosystem size is known to influence both community structure and ecosystem processes. Less is known about the evolutionary consequences of ecosystem size. A few studies have shown that ecosystem size shapes the evolution of trophic diversity by shaping habitat heterogeneity, but the effects of ecosystem size on antipredator trait evolution have not been explored. Ecosystem size may impact antipredator trait evolution by shaping predator presence (larger ecosystems have longer food chains) and habitat complexity (larger ecosystems may have more diverse habitat structure). We tested these effects using threespine stickleback from bar‐built estuaries along the Central Coast of California. These stickleback populations are polymorphic for Ectodysplasin‐A (Eda), a gene that controls bony lateral plates used as antipredator defense. We inferred Eda genotypes from lateral plate phenotypes and show that the frequency of the complete (C) allele, which is associated with greater number of lateral plates, increases as a function of ecosystem size. Predator presence and habitat complexity are both correlated to ecosystem size. The strongest proximate predictor of Eda allele frequencies was the presence of predatory fishes (steelhead trout and sculpin). Counter to expectations, habitat complexity did not have a strong modifying effect on Eda allele frequencies. Our results point to the importance of ecosystem size for determining predator presence as being the primary pathway to evolutionary effects. Ecosystem size has received much attention in ecology. Our work shows that it may be an important determinant of adaptive evolution in wild populations.

Using seasonal genomic changes to understand historical adaptation to new environments: Parallel selection on stickleback in highly‐variable estuaries

“…The threespine stickleback ( Gasterosteus aculeatus , “stickleback” hereafter) is a classic model system for studying parallel evolution (Boughman et al, 2005; Colosimo et al, 2005; Deagle et al, 2013; Haenel et al, 2019; Hendry et al, 2009, 2013; Jones, Chan, et al, 2012; Jones, Grabherr, et al, 2012; Lescak et al, 2015; Paccard et al, 2018; Smith et al, 2020). Over the past approximately 12,000 years, marine stickleback have repeatedly colonized and become adapted to freshwater environments, often through parallel phenotypic changes (Colosimo et al, 2005; Reimchen, 1983) linked to predator defence (Marchinko, 2009; Miller et al, 2019; Reimchen, 2000; Wasserman et al, 2020) and ion regulation (Gibbons et al, 2016, 2017; Hasan et al, 2017). The genomic basis of such adaptation is partly known.…”

Predator life history and prey ontogeny limit natural selection on the major armour gene,Eda, in threespine stickleback

“…Likewise, Hagen and Gilbertson (1973) reported stickleback as a prey item in 10% of rainbow trout (the same species as steelhead in this study) stomachs during spring and up to 80% during the winter. It is therefore unlikely that selection by salmonid predators directly explains the difference in Eda genotypes and plate phenotypes between estuary populations in this region (Paccard et al, 2018; Wasserman et al, 2020). However, sites with salmonids differ from those without salmonids in other ways, including the presence of predatory sculpin ( Cottus spp., Leptocottus armatus ).…”

“…Increased plate numbers and Eda "complete" allele frequencies are associated with the presence of fish predators in bar-built estuaries (Paccard et al, 2018;Wasserman et al, 2020). However, those studies did not directly observe fish consuming stickleback, and we therefore do not know how common fish predation is or how fish predation at different life stages acts on natural selection on stickleback in California estuaries.…”

“…Unlike the predominantly monomorphic populations that occur in the Pacific Northwest, stickleback in California estuaries are polymorphic for the Eda alleles leading to variation in plate morph (Baumgartner & Bell, 1984; Des Roches et al, 2020; Hagen & Gilbertson, 1973; Paccard et al, 2018). Increased plate numbers and Eda “complete” allele frequencies are associated with the presence of fish predators in bar‐built estuaries (Paccard et al, 2018; Wasserman et al, 2020). However, those studies did not directly observe fish consuming stickleback, and we therefore do not know how common fish predation is or how fish predation at different life stages acts on natural selection on stickleback in California estuaries.…”

Using seasonal genomic changes to understand historical adaptation: parallel selection on stickleback in highly-variable estuaries

“…The threespine stickleback ( Gasterosteus aculeatus , ‘stickleback’ hereafter) is a classic model system for studying parallel evolution (Boughman et al 2005; Colosimo et al 2005; Jones et al 2012a, 2012b; Deagle et al 2013; Hendry et al 2009, 2013; Lescak et al 2015; Paccard et al 2018; Haenel et al 2019; Smith et al 2020). Over the past approximately 12,000 years, marine stickleback have repeatedly colonized and become adapted to freshwater environments, often through parallel phenotypic changes (Reimchen 1983; Colosimo et al 2005) linked to predator defence (Reimchen 2000; Marchinko 2009; Miller et al 2019; Wasserman et al 2020) and ion regulation (Gibbons et al 2016, 2017; Hasan et al 2017). The genomic basis of such adaptation is partly known.…”