The Evolution of Agriculture in Beetles (Curculionidae: Scolytinae and Platypodinae)

Abstract

Beetles in the weevil subfamilies Scolytinae and Platypodinae are unusual in that they burrow as adults inside trees for feeding and oviposition. Some of these beetles are known as ambrosia beetles for their obligate mutualisms with asexual fungi--known as ambrosia fungi--that are derived from plant pathogens in the ascomycete group known as the ophiostomatoid fungi. Other beetles in these subfamilies are known as bark beetles and are associated with free-living, pathogenic ophiostomatoid fungi that facilitate beetle attack of phloem of trees with resin defenses. Using DNA sequences from six genes, including both copies of the nuclear gene encoding enolase, we performed a molecular phylogenetic study of bark and ambrosia beetles across these two subfamilies to establish the rate and direction of changes in life histories and their consequences for diversification. The ambrosia beetle habits have evolved repeatedly and are unreversed. The subfamily Platypodinae is derived from within the Scolytinae, near the tribe Scolytini. Comparison of the molecular branch lengths of ambrosia beetles and ambrosia fungi reveals a strong correlation, which a fungal molecular clock suggests spans 60 to 21 million years. Bark beetles have shifted from ancestral association with conifers to angiosperms and back again several times. Each shift to angiosperms is associated with elevated diversity, whereas the reverse shifts to conifers are associated with lowered diversity. The unusual habit of adult burrowing likely facilitated the diversification of these beetle-fungus associations, enabling them to use the biomass-rich resource that trees represent and set the stage for at least one origin of eusociality.

Phylogeny of ambrosia beetle symbionts in the genus Raffaelea

“…Massoumi Alamouti et al (2009) noted, referencing work by Cassar and Blackwell (1996) and Farrell et al (2001), that SSU-based phylogenies indicated that both Ambrosiella and Raffaelea are polyphyletic. This led these authors to suggest that the similar morphologies of the two genera and their intimate associations with ambrosia beetles arose more than once in each genus.…”

“…This led these authors to suggest that the similar morphologies of the two genera and their intimate associations with ambrosia beetles arose more than once in each genus. The ambrosial habit in beetles is also polyphyletic and has arisen at least seven times (Farrell et al 2001). …”

“…This distinction is difficult to discern microscopically, and its utility to distinguish the two genera has been questioned Oberwinkler 2005, Harrington et al 2008). Molecular phylogenetic approaches have been used to clarify the taxonomic relationships of most groups of fungi, including the Ophiostomatales (Duong et al 2012, Farrell et al 2001, James et al 2006, Slippers et al 2013. Ribosomal DNA sequence data have confirmed that the two genera are not closely related, as Raffaelea resides in the Ophiostomatales and Ambrosiella in the Microascales (Cassar & Blackwell 1996;Jones & Blackwell 1998;De Beer et al 2013a).…”

General environmental heterogeneity as the explanation of sexuality? Comparative study shows that ancient asexual taxa are associated with both biotically and abiotically homogeneous environments

“…arbuscular mycorrhizal fungi of the order Glomales (Croll & Sanders, 2009), tardigrades (Mobjerg et al., 2011; Pilato, 1979), nematode genus Meloidogyne (Castagnonesereno et al., 1993), ostracods Heterocypris incongruens (Ramdohr) and Eucypris virens (Jurine) (Butlin et al., 1998; Martens, 1998), bristle fern Trichomanes intricatum (Farrar) (Farrar, 1992), basidiomycete fungal families Lepiotaceae and Tricholomataceae (Currie, Mueller, & Malloch, 1999; Currie, Scott, Summerbell, & Malloch, 1999), ambrosia fungi Ophiostomatales (Farrell et al., 2001), or brine shrimp “ Artemia parthenogenetica ” (Bowen & Sterling) (Vanhaecke, Siddall, & Sorgeloos, 1984)—and their adaptations are similar to those of the AAs included in this study (see below).…”

“…The ant symbionts are from the basidiomycete groups Tricholomataceae and Lepiotaceae (Mueller, Rehner, & Schultz, 1998), whereas bark beetles domesticate the ambrosia fungi of the ascomycete group Ophiostomatales (Farrell et al., 2001). The association is particularly close in the ants.…”