Parallel evolution of passive and active defence in land snails

Abstract

Predator-prey interactions are major processes promoting phenotypic evolution. However, it remains unclear how predation causes morphological and behavioural diversity in prey species and how it might lead to speciation. Here, we show that substantial divergence in the phenotypic traits of prey species has occurred among closely related land snails as a result of adaptation to predator attacks. This caused the divergence of defensive strategies into two alternatives: passive defence and active defence. Phenotypic traits of the subarctic Karaftohelix land snail have undergone radiation in northeast Asia, and distinctive morphotypes generally coexist in the same regions. In these land snails, we documented two alternative defence behaviours against predation by malacophagous beetles. Furthermore, the behaviours are potentially associated with differences in shell morphology. In addition, molecular phylogenetic analyses indicated that these alternative strategies against predation arose independently on the islands and on the continent suggesting that anti-predator adaptation is a major cause of phenotypic diversity in these snails. Finally, we suggest the potential speciation of Karaftohelix snails as a result of the divergence of defensive strategies into passive and active behaviours and the possibility of species radiation due to anti-predatory adaptations.

Divergence before and after the isolation of islands: Phylogeography of the Bradybaena land snails on the Ryukyu Islands of Japan

“…In fact, clade D has significantly different shell width and height compared to clades A and F (Figure b; Table ), and there is no evidence of hybridization between these clades (Figure ). Alternative hypotheses for the shell morphology divergence in land snails include competition (Barker, ; Goodfriend, ), environmental factors (Emberton, ; Tillier, ), habitat (Hirano, Kameda, Kimura, & Chiba, ) and protection from predators (Morii, Prozorova, & Chiba, ). However, fundamental biological information for Bradybaena in the Ryukyu Islands is lacking, so further surveys to clarify what factors actually affect the shell morphology of this genus are necessary.…”

“…In fact, clade D has significantly different shell width and height compared to clades A and F ( Figure 7b; Table 3), and there is no evidence of hybridization between these clades (Figure 3). Alternative hypotheses for the shell morphology divergence in land snails include competition (Barker, 2001;Goodfriend, 1986), environmental factors (Emberton, 1982;Tillier, 1981), habitat (Hirano, Kameda, Kimura, & Chiba, 2015) and protection from predators (Morii, Prozorova, & Chiba, 2016…”

Positive or negative? The shell alters the relationship among behavioral defense strategy, energy metabolic levels and antioxidant capacity in freshwater turtles

“…Similarly, the larger plastron can offer a larger radius of protection for the ventral side of turtles when they are overturned. Thus, the variation in shell morphology matches the different behavioral defense strategies of turtle species and can also be observed in other animals that similarly carry a similar shell, such as land snails [55]. At the same time, shell morphology also linked with RMR among the three turtle species with a positive correlation (RMR vs. H/W ratio: r = 0.322, P = 0.031; RMR vs. P/C ratio: r = 0.510, P < 0.001), indicating a greater energy cost to support bigger shells.…”

Structure–behaviour correlations between two genetically closely related snail species

“…Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited. difference between passive and active strategies was found to be reflected in their shell morphology, suggesting a correlation between behaviour and shell architecture to optimize the preferred defence strategy [16]. Since no obvious difference was found in the habitat of those species, it is likely that the phenotypic and behavioural divergence were induced by predation pressure.…”

“…After that, all shells were kept in dry state. The experiments to observe the response of the snails to a predator were carried out previously and published in Morri et al [16]. The movies used to observe the response of the snails to predatory attacks from beetles can be found at this link: https://www.nature.com/articles/srep35600#Sec14.…”