The parasite-host system
Asexual morphs of the hyphomycete genera Torrubiella arachnophila(Hypocreales, Ascomycota), namely Gibellula spp ., are specialized fungal pathogens attacking primarily members of the Salticidae family of spiders (Mains, 1950; Samson and Evans, 1982, 1992). These fungi are found globally throughout the tropics and sub tropics and range into temperate climates (Evans and Samson 1987). Two species occur in North America, G. pulchra and G. leiopus (Mains 1950), the former known from as far as north as Nova Scotia, Canada (Strongman, 1991). These fungi play an important role in the regulation and maintenance of arthropod populations, especially in tropical ecosystems where they may constitute a significant mortality factor of spiders (Evans 1982; Evans and Samson 1987; Augustyniuk-Kram and Kram 2012).
Immediately prior to death, spiders infected with the speciesGibellula pulchra spin a thin flat layer of webbing on the underside of a leaf well above the forest floor, then situate themselves upon the web as if resting. The host dies shortly after taking this final position and the emergence of fungal mycelia from the feet of the host further secure the cadaver to the webbing. The fungal hyphae do not penetrate plant tissues and the leaves on which hosts die are typically healthy and without damage or leafspot (Selçuk et al. 2004). In the following days and weeks, whirling stalks of fungal hyphae bearing thousands of conidia emerge from the mummified cadaver, allowing huge numbers of the infectious propagules to disperse with wind and minor perturbation (Figure 1).
Securing of hosts to the substrata is a common feature in the final stages of many fungal entomopathogen life cycles (Hughes et al. 2010; Malagocka et al. 2015; Hughes et al 2016; Araújo and Hughes 2016). However, an interesting distinction in the case of spiders infected withGibellula pulchra is that the “death-bed” woven by the spider constitutes the substrata rather than the leaf surface. As with the “death-grip” behavior observed in Ophiocordyceps- infected ants (Anderson et al. 2009; Hughes et al. 2011), this peculiar “death-bed” behavior is not among the repertoire of web-structures built by healthy uninfected individuals, and ostensibly serves no purpose other than securing the host post-mortem. This characteristic pre-death ritual is also observed both in situ in field specimens and in laboratory specimens infected under controlled conditions. It is therefore argued that this behavior represents an extended phenotype of parasite gene expression, optimizing parasite fitness by ensuring that the hosts die securely in locations ideally suited for dispersal. Furthermore, since the act of spinning the deathbed in such specific locations represent novel behaviors absent in uninfected hosts, and which clearly benefit fungal dispersal, it is also argued that this manipulation of host behavior is adaptive for the parasite.