Size selection by a gape‐limited predator of a marine snail: Insights into magic traits for speciation

Abstract

The intertidal snail Littorina saxatilis has repeatedly evolved two parallel ecotypes assumed to be wave adapted and predatory shore crab adapted, but the magnitude and targets of predator‐driven selection are unknown. In Spain, a small, wave ecotype with a large aperture from the lower shore and a large, thick‐shelled crab ecotype from the upper shore meet in the mid‐shore and show partial size‐assortative mating. We performed complementary field tethering and laboratory predation experiments; the first set compared the survival of two different size‐classes of the crab ecotype while the second compared the same size‐class of the two ecotypes. In the first set, the large size‐class of the crab ecotype survived significantly better than the small size‐class both on the upper shore and in the laboratory. In the second set, the small size‐class of the crab ecotype survived substantially better than that of the wave ecotype both on the upper shore and in the laboratory. Shell‐breaking predation on tethered snails was almost absent within the lower shore. In the laboratory shore crabs (Pachygrapsus marmoratus) with larger claw heights selected most strongly against the small size‐class of the crab ecotype, whereas those with medium claw heights selected most strongly against the thin‐shelled wave ecotype. Sexual maturity occurred at a much larger size in the crab ecotype than in the wave ecotype. Our results showed that selection on the upper shore for rapid attainment of a size refuge from this gape‐limited predator favors large size, thick shells, and late maturity. Model parameterization showed that size‐selective predation restricted to the upper shore resulted in the evolution of the crab ecotype despite gene flow from the wave ecotype snails living on the lower shore. These results on gape‐limited predation and previous ones showing size‐assortative mating between ecotypes suggest that size may represent a magic trait for the thick‐shelled ecotype.

Life-History Multistability Caused by Size-Dependent Mortality

“…The finding that bistability can be attained for both negative and positive size dependence is particularly noteworthy, as so far theoretical research (Chase 1999;Day et al 2002;Taborsky et al 2003Taborsky et al , 2012Gårdmark and Dieckmann 2006) and empirical research (Nakaoka 1998;Chase 1999;Urban 2007Urban , 2008Engqvist and Taborsky 2016;Boulding et al 2017) on life-history bistability have focused on negative size dependence. Positively size-dependent mortality can arise by preferences of predators for larger prey (e.g., Hanson et al 1989;Wellborn 1994;Johnson and Belk 2001).…”

“…First, negatively sizedependent mortality will select for life histories with delayed reproduction, if this allows individuals to outgrow the most intense mortality risk faced at small sizes, that is, if they can reach a size refuge (e.g., Urban 2008). For example, some bivalve species start to reproduce only after reaching a refuge size threshold beyond which they are safe from their major predator (Nakaoka 1998;Boulding et al 2017). Second, life-history strategies with short juvenile growth periods (and consequently small adult body sizes) can be advantageous because they maximize the chance of reaching adulthood and accruing at least some reproductive output during their lifetime (Taborsky et al 2003).…”

Genome‐wide association analyses reveal polygenic genomic architecture underlying divergent shell morphology in SpanishLittorina saxatilisecotypes

“…Littorina saxatilis is considered a model system for the study of ecological speciation because it forms pairs of locally adapted “crab” and “wave” ecotypes across shared intertidal ranges in rocky beach sites across the Northeast Atlantic (Johannesson et al, ; Rolán‐Alvarez, Austin, & Boulding, ). These ecotypes show repeatable, parallel adaptation to crab predation or wave action in habitats within the intertidal zone (Butlin et al, ) (Boulding, Rivas, González‐Lavín, Rolán‐Alvarez, & Galindo, ; Johannesson, Johannesson, & Rolán‐Alvarez, ). Adaptive shell traits are thought to have evolved in situ despite ongoing gene flow (Butlin et al, ; Galindo, Martínez‐Fernández, Rodríguez‐Ramilo, & Rolán‐Alvarez, ; Kess, Galindo, & Boulding, ; Rolán‐Alvarez et al, ) and have been shown to mediate partial reproductive isolation between the two ecotypes with respect to shell size (Rolán‐Alvarez et al, ), implicating shell size divergence as a “magic trait” facilitating both local adaptation and assortative mating (Boulding et al, ; Galindo, Cacheda, Caballero, & Rolán‐Alvarez, ; Johannesson et al, ; Servedio, Doorn, Kopp, Frame, & Nosi, ).…”

“…Although the importance of antipredator shell traits in facilitating divergence among ecotypes has been demonstrated in L. saxatilis (Boulding et al, ), little is known about the genomic architecture underlying shell morphology (Rolán‐Alvarez et al, ). Studying the genomic basis of shell traits can provide insight into the genomic architecture that has produced local adaptation observed among L. saxatilis ecotypes despite ongoing gene flow (Johannesson, Butlin, Panova, & Westram, ).…”

Assortative mating, sexual selection and their consequences for gene flow inLittorina

“…Wave individuals live on cliffs, and they have evolved a relatively large foot, thin shell, a bold behavior and small sizes, whereas Crab snails live among boulders, and differ from the Wave snails by a larger, thicker shell with a narrower foot, showing a wary behavior. Trait differences between ecotypes, such as size and shape of the shell, are the result of local adaptation, most likely induced by wave action in the wave-exposed habitat and crab predation in the crab-rich habitat (Johannesson 1986;Boulding et al 2017;Le Pennec et al 2017). Many genomic regions potentially involved in the divergence process in L. saxatilis have been identified, including several putative inversions (Westram et al 2018;Faria et al 2019;Morales et al 2019).…”