Proteomic evidence of a paedomorphic evolutionary process within a marine snail species: a strategy for adapting to extreme ecological conditions?

Abstract

The exposed and sheltered ecotypes of the marine snail Littorina saxatilis from European rocky shores are considered a key model system to study adaptation and ecological speciation. Previous studies showed that two ecotypes (RB and SU) of this species in NW Spain have adapted differently to different shore levels and microhabitats. In order to understand how this divergent adaptive process has been accomplished, we followed a quantitative proteomic approach to investigate the proteome variation in a number of different biological factors, that is, ecotype, ontogeny and their interactions. This approach allowed testing the hypothesis that one of the ecotypes has evolved by paedomorphosis, and also whether or not the molecular mechanisms related to ecotype differentiation are set up in early developmental stages. Additionally, the identification of some candidate proteins using mass spectrometry provides some functional insights into these evolutionary processes. Results from this study provided evidence of higher ontogenetic differentiation at proteome level in the RB (metamorphic) than in SU (paedomorphic) ecotype that point to the possibility of juvenile stage retention in this latter ecotype. The level of protein expression (proteome) differences between ecotypes maintained nearly constant from late embryonic stages to adulthood, although some proteins involved in these changes considerably differed in embryonic compared to other ontogenetic stages. Paedomorphosis may be the evolutionary response of the SU ecotype of solving the trade-off during sexually immaturity that is caused by the evolution of small size arising from adaptation to the wave-exposed habitat. Some potential candidate genes of adaptation related to energetic metabolism have been identified, providing a promising baseline for future functional analyses.

Microstructural details in shells of the gastropod generaCarychiellaandCarychiumof the Middle Miocene

“…; Diz et al . ). For example, if tininess of C. eumicrum (and all Carychiella species) promoted increased survival by wedging into tight crevices to avoid predation or desiccation in extreme environmental situations, then an apparent trade‐off may have encompassed their avoidance in reaching the minimum possible size/age for sexual maturation.…”

“…Thus, in this context, a selective pressure favouring a shift towards paedomorphosis via progenesis is plausible (Diz et al . ). In a recent model, Edeline et al .…”

“…It is a frequent mechanism of phenotypic change (Gould 1977;McNamara 1997), whereby larvae do not complete metamorphosis and individuals reach sexual maturity while retaining a larval morphology. Paedomorphosis is largely driven by ecological factors (Diz et al 2012;Bonett et al 2013). Moreover, paedomorphosis via progenesis promotes early somatic maturation and an abbreviated ontogeny (Bhullar et al 2012).…”

“…Moreover, paedomorphosis via progenesis promotes early somatic maturation and an abbreviated ontogeny (Bhullar et al 2012). Although small size alone does not result in paedomorphic morphology, it has factored in discussions about the evolution of paedomorphosis (Bhullar et al 2012;Diz et al 2012). For example, if tininess of C. eumicrum (and all Carychiella species) promoted increased survival by wedging into tight crevices to avoid predation or desiccation in extreme environmental situations, then an apparent trade-off may have encompassed their avoidance in reaching the minimum possible size/age for sexual maturation.…”

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

“…This spatial escape from predation may have permitted the wave ecotype to evolve a small size at maturity, and a flat shell shape, to exploit either small cracks (Emson & Faller-Fritsch, 1976) or small biogenic refuges from heavy surf (Rickards & Boulding, 2015) created by mussel beds. Where small size in the lower shore is favored, that should concomitantly favor sexual maturity at smaller sizes by paedomorphosis (Diz, Páez de la Cadena, & Rolán-Alvarez, 2012). The wave ecotype also has a large aperture which permits a larger foot and reduces dislodgment (Trussell, Johnson, Rudolph, & Gilfillan, 1993).…”