The evolution of antipredator behaviour following relaxed and reversed selection in Alaskan threespine stickleback fish

Abstract

Changing environments, whether through natural or anthropogenic causes, can lead to the loss of some selective pressures (‘relaxed selection’) and possibly even the reinstatement of selective agents not encountered for many generations (‘reversed selection’). We examined the outcome of relaxed and reversed selection in the adaptive radiation of the threespine stickleback fish, Gasterostues aculeatus L., in which isolated populations encounter a variety of predation regimes. Oceanic stickleback, which represent the ancestral founders of the freshwater radiation, encounter many piscivorous fish. Derived, freshwater populations, on the other hand, vary with respect to the presence of predators. Some populations encounter native salmonids, whereas others have not experienced predation by large fish in thousands of generations (relax-selected populations). Some relax-selected populations have had sport fish, including rainbow trout, Oncorhynchus mykiss, introduced within the past several decades (reverse-selected). We examined the behavioural responses of stickleback from three populations of each type to simulated attacks by trout and birds to determine whether relaxed and reversed selection has led to divergence in behaviour, and whether this divergence was predator specific. Fish from trout-free populations showed weak responses to trout, as predicted, but these responses were similar to those of oceanic (ancestral) populations. Fish from populations that co-occur with trout, whether native or introduced, showed elevated antipredator responses, indicating that in freshwater, trout predation selects for enhanced antipredator responses, which can evolve extremely rapidly. Comparison of laboratory-reared and wild-caught individuals suggests a combination of learned and genetic components to this variation. Responses to a model bird flyover were weakly linked to predation environment, indicating that the loss of predation by trout may partially influence the evolution of responses to birds. Our results reject the hypothesis that the consistent presence of predatory birds has been sufficient to maintain responses to piscivorous fish under periods of relaxed selection.

Developmental timing differences underlie armor loss across threespine stickleback populations

“…The variable expressivity of the low-pelvis phenotype we see in DER2 could be due to epistasis such as among identified modifier loci and pitx2 (Bell et al, 2007;Cresko et al, 2004;Marcil, 2003;Peichel et al, 2001;Shapiro et al, 2004), due to subtle environmental perturbation despite our controlled rearing conditions, or due to stochasticity in expression networks such as might be caused by a near-threshold level of pitx1 or downstream targets. That low-pelvis fish still harbor developmental competence to generate components of the pelvic apparatus, such as was observed here and by others (e.g., Bell et al, 2007) and was functionally tested by Chan et al (2010), suggests a potential for atavism or novel pelvic modification even in lineages with deleted pitx1 enhancer alleles, such as in Boot Lake ( Figure S8 in Chan et al, 2010), which has recently experienced an influx of novel predators (Wund et al, 2015).…”

“…Such change in stickleback can take place even on the order of decades (Hagen & Gilbertson, 1973;Klepaker, 1993;Bell, 2001;Bell & Aguirre, 2013;Bell, Aguirre, Buck, & Wainwright, 2004;Bell et al, 2016;Lescak et al, 2015;Terekhanova et al, 2014). The different demands of alternative habitats for predation survival, locomotion, and feeding are reflected in modified behavioral, defensive armor, fin, body shape, and cranial traits (Bell & Foster, 1994;Hagen & Gilbertson, 1972;Huntingford, Wright, & Tierney, 2004;Kimmel et al, 2012;Reimchen, 1994;Walker, 1997;Walker & Bell, 2000;Wund, Baker, Golub, & Foster, 2015).…”

Shift in predation regime mediates diversification of foraging behaviour in a dragonfly genus

“…The loss and reduction of anti-predator traits have been intensively studied in populations invading new habitats (e.g. Vamosi & Schluter, 2002;Harris et al, 2011;Wund et al, 2015;Mikolajewski et al, 2015a;Stoks et al, 2016) as well as in populations colonising islands (e.g. Blumstein & Daniel, 2002;Vervust et al, 2007;Pafilis et al, 2009;Runemark et al, 2014).…”

Iterative development and the scope for plasticity: contrasts among trait categories in an adaptive radiation

“…Particularly well studied in the context of individual variation within and between populations is the shy/bold behavioral continuum (Huntingford, 1976;Wilson et al, 1994;Bell and Sih, 2007;Dingemanse et al, 2007). The origins of these differences are not well explored to date, although there is evidence for both genetic and learned contributions in threespine stickleback (Bell and Stamps, 2004;Bell and Sih, 2007;Dingemanse et al, 2007;Wund et al, 2015), and one experimental study provided clear evidence that experience with predators could organize syndromes (Bell and Sih, 2007). Whether behavioral syndromes that present as a consequence of experience are persistent or reversible has not to our knowledge been examined, although the experiment by Bell and Sih (2007) makes clear that the organization of such syndromes is activational in that presumably the same neural network can produce alternative outcomes over relatively short time frames.…”