Genetic Variation of the Shell Morphology in Acanthina Monodon (Gastropoda) in Habitats with Different Wave Exposure Conditions
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Vol. 18: 253–260, 2013 AQUATIC BIOLOGY Published online June 4 doi: 10.3354/ab00508 Aquat Biol Genetic variation of the shell morphology in Acanthina monodon (Gastropoda) in habitats with different wave exposure conditions Maribel R. Solas1, Roger D. Sepúlveda2, Antonio Brante1,* 1Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Casilla 297, Concepción, Chile 2Instituto de Ciencias Ambientales y Evolutivas, Facultad de Ciencias, Universidad Austral de Chile, Casilla 567, Valdivia, Chile ABSTRACT: Shell morphology in marine gastropods exhibits high intraspecific variability. Plasti- city appears to be the most common response; however, additive genetic variance would explain a significant amount of morphological variance promoting local adaptations. The marine gastro- pod Acanthina monodon is a direct developer with a low dispersal potential and high variability in shell morphology. Previous studies suggest that adult shell morphology could have an adaptive value that responds to the degree of wave exposure. Given the low dispersal potential of A. mono - don and the high temporal predictability of wave exposure conditions at the local scale, it was expected that selection would favour local adaptations with an important component of heritabil- ity. To test this hypothesis we estimated shell morphology heritability of A. monodon using pre- hatching juveniles from wave-exposed and wave-sheltered sites along the Chilean coast and using a geometric morphometrics approach. In addition, we compared shell morphology and size of pre-hatching juveniles between exposed and sheltered sites. Heritability of shell morphology was highly variable, ranging between 0.2 and 0.6 among sites. Shell morphology of pre-hatching individuals did not differ between exposed and sheltered conditions. These results suggest that the diversity of shell morphology in adults of A. monodon could be explained by a complex inter- action between plastic and heritable responses. KEY WORDS: Additive genetic variance · Phenotypic plasticity · Geometric morphometrics · Snail · Shell shape · Body size Resale or republication not permitted without written consent of the publisher INTRODUCTION on how individuals perceive the habitat. In species with high dispersal potential, a high proportion of Natural selection can produce adaptations to dif- heritability will evolve in environments with low ferent habitats in 2 ways: first, by direct action on spatial and temporal variability; on the other hand, the additive genetic component, and second, by a high proportion of plasticity would be advanta- phe no typic plasticity (Via 1993, Via et al. 1995, geous in habitats with high spatial or temporal Kingsolver et al. 2002). Theoretical models suggest variability. In contrast, in species with low disper- that the proportional influence of each component sal, high levels of inheritance would be advanta- (genetic and plasticity) on a trait will depend on geous in local environments with low temporal genetic flow intensity and environmental un cer - variability. Thus, the study of inheritance and plas- tainty (Bertness & Gaines 1993, Mopper et al. ticity evolution must incorporate both the environ- 1995, Holt & Gomul kie wicz 1997). Thus, the evolu- mental characteristics and life history strategies of tion of the optimal genetic/plastic ratio will depend species in order to understand adaptation and spe- *Corresponding author. Email: [email protected] © Inter-Research 2013 · www.int-res.com 254 Aquat Biol 18: 253–260, 2013 ciation processes at ecological and evolutionary to wave action and more elongated at sheltered sites, scales (Zelditch et al. 2004). resulting in 2 ecotypes (Kitching et al. 1966, Crothers Morphology is usually a feature related to fitness, 1975, Rolán et al. 2004). Individuals from exposed and is therefore restricted to strong selective pres- sites are characterized by a more rounded aperture sures (Johannesson et al. 1993). Shell morphology of with a larger foot which facilitates a stronger attach- marine gastropods has been one of the most fre- ment to the substrata (Kirby et al. 1994). Both species quently studied morphological traits, due to its are direct developers, which means they lack an importance for taxonomic and evolutionary studies. intermediate larval stage, and display a restricted At the intraspecific-level, shell morphology exhibits crawling range. Moreover, genetic analyses indicate high polymorphism, which is explained by both envi- a low dispersal potential (Pascoal et al. 2012). The ronmental and biological factors. For example, the characteristics of the selective forces, such as wave intertidal species Littorina saxatilis and Nucella lapil- strength, which usually exhibits high local pre- lus exhibit a high degree of variability in shell mor- dictability over time (a site may be classified as ex - phology, resulting in several morphs or ecotypes posed or sheltered depending on the strength of tem- apparently related to local selective pressures in - poral wave patterns), and their restricted dispersal duced by environmental conditions such as preda- suggest that the shell morphology of these species tion and wave strength (Johannesson et al. 1993). In should have a high genetically additive base, with N. lapillus the shell is more globular at sites exposed significant heritability values. In fact, for L. saxatilis Fig. 1. (A) Location of the wave-exposed and -sheltered sites along the central Chilean coast. Wave-sheltered sites: Hualpén A, Ramuntcho and La Misión; wave-exposed sites: Hualpén B, Tumbes and Mehuín. (B) Morphological types of Acanthina monodon adult shells in (a) wave-sheltered and (b) wave-exposed sites. (C) Morphological landmark positions used on the ventral aspect of A. monodon shell pictures Solas et al.: Heritability in marine snail shell morphology 255 and N. lapillus, heritability of the shape and size of ity. In addition, if shell morphological differences the shell have been estimated to be between 0.4 and observed in adults of A. monodon between exposed 0.7 (Johannesson & Johannesson 1996, Carballo et al. and sheltered sites do not persist in pre-hatching off- 2001, Conde-Padín et al. 2007a). Despite the impor- spring, this would indicate that plasticity appears to tance of the study of shell morphology in gastropods be the main mechanism responding to wave exposi- in understanding adaptive and speciation processes, tion. In this study, using a geometric morphometrics few studies have been conducted with this group, approach, we estimated shell morphology heritabil- which makes it difficult to determine the more gen- ity in A. monodon with a full sibling design using eral mechanisms and patterns that explain diversity. pre-hatching juveniles in 6 localities with different The marine gastropod Acanthina monodon (Pallas, wave strengths, and we compared size and shell 1774) is a muricid species endemic to the southeast- morphology of offspring between sites with high and ern Pacific Ocean, inhabiting intertidal rocky shores low wave exposition. and the shallow subtidal from 28 to 55° S (Gallardo 1979, Valdovinos 1999). A. monodon is dioecious with internal fertilization; females enclose their off- MATERIALS AND METHODS spring in capsules attached to hard substrata. This species has direct development and juveniles of Study area and sampling collection approximately 0.82 to 1.3 mm hatch from the cap- sules after 60 to 80 d of intracapsular development During spring 2010 we collected capsules con - (Gallardo 1979). Thus, in the absence of a pelagic taining pre-hatching juveniles of Acanthina mono - larva, the potential for dispersal in A. monodon ap - don from 6 intertidal rocky shores on the Chilean pears to be very low, and, consequently, it has a high coast: 3 wave-sheltered sites: Hualpén-Sheltered level of population genetic structure (Sánchez et al. (36° 48’ 23.07” S, 73° 10’ 36.17” W), Ramuntcho (36° 2011). Moreover, 2 genetic phylogeographic breaks 47’ 12.60” S, 73° 11’ 12.55” W) and La Misión (39° 48’ were observed at 30° S and between 41 and 53° S 45.42” S, 73° 24’ 1.65” W), and 3 wave-exposed sites: defining a northern, central and southern phylogeo- Hualpén-Exposed (36° 48’ 17.12” S, 73° 10’ 45.68” W), graphic area. This species exhibits a high degree of Tumbes (36° 43’ 04.96” S, 73° 07’ 20.34” W) and Me - variation in shape, colour and thickness of the shell huín (39° 25’ 31.29” S, 73° 13’ 00.18” W; Fig. 1A). All within and between phylogeographic areas, suggest- sites were located in the central phylogeographic ing local adaptations. Previous studies have sug- area (Sánchez et al. 2011) in order to reduce potential gested that shell morphology in this species would be differences or bias in heritability patterns between an adaptive response to predation risk and the exposed and sheltered sites due to population degree of wave exposure varying at latitudinal and genetic structure. To determine the exposure levels local spatial scales (Sánchez et al. 2011, Sepúl veda & at different sites, we used spheres made of dental Ibáñez 2012, Sepúlveda et al. 2012). For example, resin of approximately 240 g each placed in the inter- Sánchez et al. (2011) and Sepúlveda & Ibáñez (2012) tidal. Exposure was determined as a function of found that adult individuals coming from sheltered degradation of the spheres after 48 h of exposure to inner channels in the south of Chile show longer the wave action in the intertidal zone where the cap- spires, thinner shells and ornamented lips, compared sules were collected. to individuals from the northern sites. In addition, at In each site we sampled between 8 and 12 different a local scale, adults from localities with different capsule clutches (hereafter ‘families’), and 3 capsules wave exposure strengths and separated by only a at pre-hatching stage were collected per clutch. In couple of kilometres presented morphological differ- the laboratory, capsules were dissected under a ences, with a larger opercular area at the most ex - binocular microscope, and the pre-hatching juve- posed site (Fig. 1B). According to preliminary re sults, niles were stored in ethanol for posterior analyses.