Ecological Archives E094-241-A2

Junji Konuma, Teiji Sota, Satoshi Chiba. 2013. A maladaptive intermediate form: a strong trade-off revealed by hybrids between two forms of a snail-feeding beetle. Ecology 94:2638–2644.

Appendix B. Detailed description of the carabid beetles, land snails, and trade-offs in previous studies.

Carabid beetles

The carabid beetle D. blaptoides is endemic to the Japanese Archipelago and feeds on land snails for larval development and egg reproduction. This species is classified into seven subspecies (Konuma et al. 2011). Six subspecies have long, narrow heads and thoraces, whereas individuals of another subspecies, D. b. capito on Sado Island (Appendix A), have short, wide heads and thoraces. In the present study, we used D. b. capito and the most phylogenetically close subspecies, D. b. fortunei, although a different pair of stout and slender subspecies (D. b. capito and D. b. oxuroides) was used to demonstrate the functional trade-off in our previous study (Konuma and Chiba 2007). This is because we intended to use their hybrids (Konuma et al. 2013), and because we intended to confirm the repeatability of the same trade-off using another pair of D. blaptoides subspecies.

Land snails

In a previous study, we investigated which types of land snails (prey) are important for morphological diversification between stout and slender body shapes in D. blaptoides beetles (predators); we concluded that two types of land snails are key (Konuma and Chiba 2007). Compared to slender beetles, stout beetles had higher feeding performances in feeding tests with Discus pauper, Cochlicopa lubrica, Stereophaedusa japonica, and Aegista (Plectotropis)pannosa snails, all of which commonly have thin shells and small shell apertures (Fig. 4 in Konuma and Chiba 2007). In contrast, slender beetles exhibited higher performances in tests with Euhadra quaesita and Satsuma japonica, which have thick shells and large shell apertures. Neither stout nor slender beetles can eat snails with thick shells and small shell apertures such as Zaptychopsis buschi because neither shell-crushing nor shell-entry is effective in consuming these snails. In contrast, both stout and slender beetles can eat snails with thin shells and large shell apertures such as Acusta despecta sieboldiana, Bradybaena similaris, and Succinea lauta because both feeding behaviors are effective for these snails. Thus, the thin-shelled snail species with small apertures and the thick-shelled snail species with large apertures highlight the differences in feeding performance between stout- and slender-shaped beetles, whereas the other types of snail species are either unsuitable food sources for the beetles or eaten without specialized feeding techniques and may not be considered important prey for feeding specialization. The two important types of snail species (including D. pauper, St. japonica, E. quaesita, and Sa. japonica) occur on both Sado and Awashima islands, which are inhabited by D. b. capito and D. b. fortunei, respectively, whereas the small thin-shelled snail, C. lubrica, occurs only on Sado, the island inhabited by D. b. capito.

We have also suggested that morphological diversification of D. blaptoides has been especially affected by the shell-size composition of the genus Euhadra, a group of relatively large snail species (Konuma et al. 2011). Three Euhadra species occur on the islands inhabited by D. b. capito and D. b. fortunei. Euhadra sadoensis, E. brandtii, and E. quaesita inhabit Sado Island, whereas only E. quaesita occurs on Awashima Island. Of these, E. sadoensis and E. brandtii would not be important resources for the evolution of the beetle morphology, as these species are arboreal and would seldom be eaten by the ground beetle D. blaptoides. In contrast, E. quaesita is a typical ground-dwelling snail, and D. blaptoides frequently consumes this species in nature. Although E. quaesita is widely distributed in the northern Honshu area as well as on Sado and Awashima islands, a recent phylogenetic analysis using mitochondrial DNA markers suggested that E. quaesita recently colonized Sado Island from Honshu, likely due to human activity (Davison and Chiba, unpublished data). Thus, recently colonized E. quaesita and the other arboreal Euhadra species may not have served as major prey for D. blaptoides on Sado Island, whereas E. quaesita has probably been a main prey item for the beetles on Awashima Island and adjacent areas of Honshu.

To measure performance during shell-crushing, we examined the feeding success rates of beetles foraging on a small snail species, D. pauper. Because the shell apertures of these snails are much smaller than the size of the beetle’s head, we expected that beetles would not be able to insert their heads into the shells and would only be able to eat the snails by crushing their shells (Konuma and Chiba 2007). In contrast, to measure shell-entry performance, we used a large snail species, E. quaesita. The shells of these snails are so thick that beetles cannot readily crush them. Because beetles can eat this snail by inserting their heads into the shell, the feeding success rate can be considered equivalent to the performance level of shell-entry (Konuma and Chiba 2007). We were unable to examine feeding performances for the other land snails, as collecting sufficient numbers of these snails was difficult for experiments that required 120 beetle samples. However, D. pauper and E. quaesita are the representative thin-shelled snails with small shell apertures and thick-shelled snails with large shell apertures, respectively (see Fig. 3 in Konuma and Chiba 2007). Therefore, these two snails would be appropriate prey species for measuring foraging performances by shell-crushing and shell-entry.

Viability loss

Viability loss due to genetic incompatibility can potentially affect the feeding performance of hybrid beetles (Hatfield and Schluter 1999, Berlocher and Feder 2002). To examine this effect, we maintained the beetles under conditions similar to the wild environment and monitored their survival rates for 1 year, which constitutes the life span of these beetles (Sota 1985). We compared survival rates after 1 year among five populations (P1, P2, F1, B1, and B2) using G-tests. Most of the hybrid beetles (>91%) survived the 5-month overwintering period during which no food was provided. No difference in survival rate was observed after 1 year among the five populations (G-test, P > 0.05). This result suggest that viability loss due to genetic incompatibility did not largely affect the results of feeding experiments and that the reductions in snail-feeding performance of hybrid beetles were strongly affected by their intermediate body shape. However, viability is not the sole measure of genetic incompatibility, and other sources of genetic incompatibility associated with snail-feeding performances of hybrid beetles must be examined.

Trade-off curves in the previous studies

Many theoretical models of ecological specialization implement trade-offs using simple power functions (ex., Abrams 1986, 2006a, 2006b, 2006c, Meszéna et al. 1997, HilleRisLambers and Dieckmann 2003, Egas et al. 2004, Spichtig and Kawecki 2004, Rueffler et al. 2006a, Ravigné et al. 2009). For example, the feeding performances of predators with phenotypic values x for prey-type 1 and prey-type 2 are assumed to be as follows, respectively:


where f1max and f2max are positive constants. The (f1, f2) plot is a curve with a negative slope (Fig. 1A), which implies that trade-offs exist between the two fitness components. The shape of curves is determined by the positive parameter s. The curves bend outward when s > 1 (line (1) in Fig. 1A) and bend inward when s < 1 (lines (3) and (4) in Fig. 1A). The former curves represent weak trade-off, while the latter curves represent strong trade-off.


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