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BMC Evolutionary Biology Biomed Central BMC Evolutionary Biology BioMed Central Research article Open Access Why do snails have hairs? A Bayesian inference of character evolution Markus Pfenninger*1, Magda Hrabáková2, Dirk Steinke3 and Aline Dèpraz4 Address: 1Abteilung Ökologie & Evolution, J.W. Goethe-Universität, BioCampus Siesmayerstraße, 60054 Frankfurt/Main, Germany, 2Deparment of Zoology, Charles University, Viniènà 7, 128 44 Praha 2, Czech Republic, 3Department of Biology, University of Konstanz, Postbox 5560 M618, 78457 Konstanz, Germany and 4Département d'Ecologie et Evolution, Université de Lausanne, Bâtiment de Biologie, Dorigny, 1015 Lausanne, Switzerland Email: Markus Pfenninger* - [email protected]; Magda Hrabáková - [email protected]; Dirk Steinke - [email protected]; Aline Dèpraz - [email protected] * Corresponding author Published: 04 November 2005 Received: 14 July 2005 Accepted: 04 November 2005 BMC Evolutionary Biology 2005, 5:59 doi:10.1186/1471-2148-5-59 This article is available from: http://www.biomedcentral.com/1471-2148/5/59 © 2005 Pfenninger et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Abstract Background: Costly structures need to represent an adaptive advantage in order to be maintained over evolutionary times. Contrary to many other conspicuous shell ornamentations of gastropods, the haired shells of several Stylommatophoran land snails still lack a convincing adaptive explanation. In the present study, we analysed the correlation between the presence/absence of hairs and habitat conditions in the genus Trochulus in a Bayesian framework of character evolution. Results: Haired shells appeared to be the ancestral character state, a feature most probably lost three times independently. These losses were correlated with a shift from humid to dry habitats, indicating an adaptive function of hairs in moist environments. It had been previously hypothesised that these costly protein structures of the outer shell layer facilitate the locomotion in moist habitats. Our experiments, on the contrary, showed an increased adherence of haired shells to wet surfaces. Conclusion: We propose the hypothesis that the possession of hairs facilitates the adherence of the snails to their herbaceous food plants during foraging when humidity levels are high. The absence of hairs in some Trochulus species could thus be explained as a loss of the potential adaptive function linked to habitat shifts. Background shell structures [3,4] and have attracted considerable Evolutionary theory predicts that costly structures must research efforts to explain them in adaptive terms [5-7]. convey a fitness advantage to their bearers in order to be The proposed roles invoked mechanical stability [8], maintained over evolutionary time [1]. Flightlessness in defence against predators [9], sexual selection [10] and birds and insects, limblessness in lizards and sightlessness climatic selection [11]. However, the potential selective in cave-dwelling organisms are some prominent examples advantage of hair-like shell ornamentation of certain land of phenotypic regression due to the loss of adaptive func- snail species remains unknown. tion (reviewed in [2]). Molluscs in general and gastropods in particular display a fascinating diversity of elaborate Page 1 of 11 (page number not for citation purposes) BMC Evolutionary Biology 2005, 5:59 http://www.biomedcentral.com/1471-2148/5/59 TVJ1 1.00 TVJ3 TVJ4 Trochulus villosulus TVJ6 D3 2 1.00 D3 4 D4 2 Lineage A D4 1 D4 3 1.00 MdO1 1 Lineage B MdO1 3 1.00 D5 7 D7 8 Lineage C D6 1 D7 1 TB1 1.00 TB2 TB3 Trochulus biconicus TB4 TA1 0.88 TA2 Trochulus alpicolus 1.00 TA3 TA4 0.75 CH13 4 Trochulus villosus CH13 6 1.00 PLB1 PLB2 Trochulus lubomirskii CH21 5 0.99 CH21 4 CH21 3 Trochulus caelatus CH21 6 0.67 CH21 2 CH11 1 CH11 2 1.00 CH11 7 CH11 10 1.00 CH12 1 Trochulus montanus CH10 1 CH10 2 0.97 CH10 9 CH11 6 CH10 4 CH3 3 CH3 5 0.91 0.99 CH18 5 Trochulus clandestinus CH3 2 CH18 1 1.00 MdO1 4 Lineage D MdO1 5 CH24 8 0.99 CH21 1 CH24 4 Lineage E CH24 6 CH24 7 CH6 1 CH6 2 1.00 CH8 2 Lineage F CH8 3 CH8 9 CH8 10 1.00 CH8 1 Lineage G CH8 7 1.00 CH15 4 Lineage H 0.61 0.55 CH15 8 D7 6 1.00 D7 9 Lineage I 1.00 D8 3 D8 6 CHAT 9 CHAT 10 1.00 CHAT2 Trochulus nov. spec. CHAT1 CHAT3 0.1 CHAT4 UnrootedFigure 1 consensus tree of 90,000 trees sampled by the Markov-chain in Bayesian analysis for the COI-fragment Unrooted consensus tree of 90,000 trees sampled by the Markov-chain in Bayesian analysis for the COI-frag- ment. Numbers on nodes indicate the Bayesian posterior probability. Page 2 of 11 (page number not for citation purposes) BMC Evolutionary Biology 2005, 5:59 http://www.biomedcentral.com/1471-2148/5/59 These hairs can reach varying densities (up to 20 per Trochulus within the Hygromiinae with high posterior squaremilimetre) and lengths (up to three millimetres). probability, except for T. lubomirskii, which seems to be In some cases hardly visible, they confer an almost furry only distantly related to this genus (Figure 2). In addition impression to the shell in others. These semi-rigid struc- to the early branching T. villosus/alpicolus clade, the genus tures are part of the periostracum, a thin protein layer is composed of three well supported subclades: first, a (conchiolin) secreted by the snail to cover the calcareous clade containing the T. striolatus/plebeius-like lineages shell [12]. Building hairs requires the snail to have special- together with T. villosulus, a second clade with ecologically ised glandular tissue and complex strategies to form them. divers species confined to the Jura mountains and the Consequently, this trait can be assumed to be costly and neighbouring Mittelland-plain and finally, a T. hispidus/ should thus present a selective advantage to its bearers in sericeus-like clade, containing also T. biconicus and a new order to be conserved. species. Haired shells occur in several species of the Stylommato- Correlation of shell hairiness with habitat phoran families Polygyridae, Helicidae and Hygromiidae. The PCA on habitat humidity describing variables These families are only distantly related [13], suggesting resulted in two meaningful axes, representing 79.7% and that this features has evolved several times independently. 13.4% of the total variation. The first component opposed Haired shells are almost exclusively observed in species sampling sites in shady woods and sites in sun exposed, living in moist microhabitats, like layers of fallen leaves, open areas. This axis can therefore be interpreted as an broad-leaved vegetation, damp meadows or wet scree evaporation gradient. The second axis is a gradient of the [14]. Such a correlation suggests an adaptive significance summer precipitation on one hand and the humidity of the trait in such a habitat [1]; it was thus speculated that demand of the vegetation on the other (Figure 3). It can the hygrophobic hairs facilitate the movement in wet thus be considered as a humidity gradient. The sampling environments by relieving surface tension [14,15]. A cor- sites appear as two distinct clusters that could be classified relation between haired shells and humid habitats is thus as either moist or dry (Table 1). The outlier (TA) was also expected. In order to test this, we employed the recent considered to be humid, according to its high humidity Bayesian extensions of the comparative method, allowing levels. For each population, at least ten adult individuals to take mapping and phylogenetic uncertainty simultane- were scored for the presence or absence of hairs (mixed ously into account [16]. With a diversity hotspot in South populations were not found). Non-haired populations Germany, Eastern France and Switzerland, the land snail exclusively corresponded to species described in the liter- genus Trochulus s. str. (common name: Hairy snails) is par- ature as having smooth shells (Table 1). When plotting ticularly suited to address our question: its species exhibit the hairiness of each population on the PCA, a complete variability in both hairiness and ecology. This study congruence between humidity and hairiness became present the first comprehensive molecular phylogeny for apparent: haired shells tended to occur at sites with low the genus Trochulus Chemnitz, 1786 (until recently evaporation and/or high precipitation while smooth Trichia, Hartmann 1840) based on mitochondrial and shells were found at places with high evaporation and/or nuclear loci. Finally, we tested experimentally whether the lower precipitation (Figure 3). possession of haired shells indeed facilitates locomotion. Character state evolution Results As the occurrence in moist habitats was systematically Lineage identification and phylogenetic relations linked to the presence of hairs in Trochulus s.str., only a The initial phylogenetic analysis on a COI data set of the single analysis was necessary for both characters. The presumed Trochulus species resolved 18 terminal clades, Bayesian analysis of character evolution suggested with each with 0.99 posterior probabilities or higher (Figure high posterior probability that the most recent common 1). The uncorrected sequence divergence among those ancestor of the genus Trochulus most likely possessed hairs clades ranged from 0.029 to 0.173 (Table 2). Out of these and lived in a moist habitat (Figure 4). The analysis also lineages, nine could be assigned to existing taxa, because revealed considerable mapping- and/or phylogenetic the species were sampled from the type locality and/or uncertainty in the reconstruction of crucial ancestral were morphologically unmistakable. The nine remaining nodes (nodes 1–3 in Figure 4).
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