Flies that attack polymorphic snails on coloured backgrounds: selection for crypsis by a sarcophagid parasitoid of Littoraria filosa

Abstract

Many species of arboreal marine snails in the genus Littoraria are polymorphic for shell colour, with morphs that correspond in both colour and frequency to those predominant in the habitat. Although the combined effects of selection for crypsis and apostasy have been suggested as the most likely reasons for this, they have not been demonstrated directly in the field. We investigated whether two parasitoid flies, Sarcophaga megafilosia and Sarcophaga meiofilosia, select for crypsis in Littoraria filosa. It was possible to compare the proportions that matched and did not match the background between samples of live and dead snails because the shells of individuals killed by these parasitoids, within which the larva and pupa develop, remain attached to the substratum. This comparison was necessary because these snails frequently move among different coloured microhabitats, which will tend to obscure any effect of selection for crypsis if only live individuals are censused. The method appeared reliable since there was no change in background colour and very little loss of shells between larviposition and emergence of flies. S. megafilosia killed a significantly greater than expected proportion of snails that did not match their background. In contrast, there was no evidence of selective attack by S. meiofilosia. These results are discussed in relation to previous work on polymorphisms in Littoraria species. We also suggest that the role of parasitoid insects as selective agents contributing to the maintenance of colour polymorphisms in terrestrial molluscs may have been overlooked. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society, 2002, 77, 367−377.

Apostasy and selection for crypsis in the marine snail Littoraria filosa: an explanation for a balanced colour polymorphism

“…with branches that did not interlock with their neighbours. There are three broad shell colour morphs of L. filosa in Queensland (Reid, 1986, 1987), but only 7.4% of a sample of more than 3000 from our study sites were pink (McKillup & McKillup, 2002), hence this morph was not used.…”

“…The colour polymorphism in Littoraria filosa (Sowerby) has been studied in Queensland, Australia, by Hughes & Jones (1985), Hughes & Mather (1986), Reid (1987, 1992), Parsonage & Hughes (2002) and McKillup & McKillup (2002). Yellow, brown, and pink shells were present at all sites and, although the genetics of L. filosa has not been investigated, Reid (1987) noted that discrete shell colour morphs were present within groups of snails on the same tree and did not change in appearance during growth, thus suggesting a genetic basis for the polymorphism.…”

“…Parsonage & Hughes (2002) also found indirect evidence of selection for crypsis in L. filosa as the proportion of yellow snails decreased on trees where the proportion of brown in the background had been increased by pruning leaves. McKillup & McKillup (2002) found direct evidence that the sarcophagid fly Sarcophaga megafilosia Pape, McKillup & McKillup selects for crypsis in L. filosa. This parasitoid killed a significantly greater than expected proportion of yellow snails than were naturally present on grey/brown trunks, with the converse on yellow/green leaves.…”

Phylogeny ofHeteronychia: the largest lineage ofSarcophaga(Diptera: Sarcophagidae)

“…According to Keilin (), Sarcophagidae associated with snails are either saprophagous or ‘doubtful parasites’; Villeneuve () hypothesized that saprophagous or necrophagous life habits may have evolved from an original parasitic strategy. Possible true parasitoids of snails may well exist amongst the flesh flies, as in the cases exemplified by Rostand () for Sarcophaga ( Heteronychia ) filia Rondani, by Lopes () for Titanogrypa ( Sarconeiva ) fimbriata (Aldrich), by Muma (, ) and Reeves, Pape & Adler () for Lepidodexia ( Johnsonia ) elegans (Coquillet), by Stegmaier () for Helicobia morionella (Aldrich) and Peckia ( Sarcodexia ) lambens , by Lopes () for Lepidodexia ( Notochaeta ) malacophaga (Lopes), by Coupland & Baker () for Sarcophaga ( Heteronychia ) villeneuveana (Enderlein), by McKillup & McKillup (, , ) and McKillup, McKillup & Pape () for Sarcophaga ( Sarcorohdendorfia ) megafilosia Pape, McKillup & McKillup and Sarcophaga ( Sarcorohdendorfia ) meiofilosia Pape, McKillup & McKillup, by Pérez‐Moreno () for Sarcophaga ( Heteronychia ) javita (Peris, González‐Mora & Mingo), and by Sinha & Nandi (, as Liosarcophaga choudhuri [sic]) for Sarcophaga choudhuryi .…”

Adaptive responses of independent traits to the same environmental gradient in the intertidal snail Bembicium vittatum

“…Independent of its association with colour, shell spotting shows a weaker association with habitat, but still with repeatability. Studies of shell colour in intertidal gastropods have explained associations with habitat in terms of the two obvious selective mechanisms: (1) crypsis favoured by selective predation (Reid, 1987;Byers, 1995;Johannesson and Ekendahl, 2002;McKillup and McKillup, 2002;Parsonage and Hughes, 2002); and (2) thermal selection (Harris and Jones, 1995;Yeap et al, 2001;Parsonage and Hughes, 2002). Either mechanism could apply in the case of B. vittatum.…”