Macroevolution and shifts in the feeding biology of the New World scarab beetle tribe Phanaeini (Coleoptera: Scarabaeidae: Scarabaeinae)

Abstract

The New World scarab beetle tribe Phanaeini contains coprophagous, necrophagous, mycetophagous and suspected myrmecophilous species. We analyse the largest tribal molecular dataset assembled, incorporating, for the first time, the enigmatic monobasic genus Megatharsis, the thalassinus group of the subgenus Coprophanaeus (Metallophanaeus), and the subgenus Dendropaemon (Eurypodea) (formerly Tetramereia), unveiling their macroevolutionary and biogeographical history in light of Cenozoic abiotic changes and inferring shifts in feeding biology through time. We recover the contentious genus Gromphas outside an otherwise monophyletic Phanaeini. We infer Megatharsis in a clade containing the apparent myrmecophilous genus Dendropaemon, within the Coprophanaeus clade, and demonstrate that the subgenus Coprophanaeus (Metallophanaeus) is polyphyletic, whilst species groups within the subgenus Coprophanaeus (Coprophanaeus) are monophyletic. Our divergence time analyses and ancestral range estimation indicate an eastern South American origin for Phanaeini in the early Eocene, with subsequent colonization of Central America and the Nearctic during the Oligocene, long before a Panamanian land bridge. A shift to necrophagy in Coprophanaeus is possibly linked to increasing Neotropical small vertebrate diversity since the Eocene and, astonishingly, myrmecophily evolved from necrophagy 35 Mya. These drastic shifts in lifestyle are not concordant with variations in diversification rates and appear unlinked to Quaternary extinction of large mammals.

Paleogene forest fragmentation and out‐of‐Africa dispersal explain radiation of the Paleotropical dung beetle tribe Epactoidini trib. nov. (Coleoptera: Scarabaeinae)

“…Another mechanism is the Gomphotherium forest corridor that mediated the dispersal of Epactoidini to Oriental Region from Africa. Transoceanic and transcontinental dispersals shaped the current distribution of various Scarabaeinae clades (Cupello et al, 2020; Gillett & Toussaint, 2020; Gunter et al, 2019; Sole et al, 2011; Sole & Scholtz, 2010). The exclusively Paleotropical disjunct distribution of the tribe Epactoidini is remarkable within the subfamily Scarabaeinae.…”

“…Alternatively, it is logical to propose the existence of multiple corridors that might have been separated in time due to oscillating aridification events.Summing up, our study suggests that that the current distribution of Epactoidini was predominantly shaped by the interplay of two mechanisms. One is the routine transoceanic dispersal events: two such events have mediated the overwater migration of Epactoidini ancestors from Africa to Madagascar and further to Réunion island.Another mechanism is the Gomphotherium forest corridor that mediated the dispersal of Epactoidini to Oriental Region from Africa.Transoceanic and transcontinental dispersals shaped the current distribution of various Scarabaeinae clades(Cupello et al, 2020;Gillett & Toussaint, 2020;Gunter et al, 2019;Sole et al, 2011;Sole & Scholtz, 2010). The exclusively Paleotropical disjunct distribution of the tribe Epactoidini is remarkable within the subfamily Scarabaeinae.The use of the Gomphotherium corridor as dispersal route has never been previously proposed for any other dung beetle clade.Members of the tribeEpactoidini are obligate forest-dwellers, which makes them habitat specialists.…”

Taxonomic revision of the Phanaeus endymion species group (Coleoptera: Scarabaeidae), with the descriptions of five new species

“…nov., P. zapotecus and P. zoque). Apparently, the diversification of the P. endymion species group and its dispersal to the Mexican temperate forests started during the Miocene (Price 2009;Kohlmann et al 2018;Gillett & Toussaint 2020).…”

“…On the other hand, the P. endymion species group is the only one within Phanaeus that successfully shifted from coprophagy to necrophagy, mycetophagy and saprophagy (Halffter & Matthews 1966;Edmonds 1994Edmonds , 2003Edmonds , 2006Halffter & Halffter 2009;Deloya et al 2013;Gillett & Toussaint 2020).…”

“…We followed the nomenclature proposed by Harris (1979), Edmonds (1994) and Cristóvão & Vaz-de-Mello (2020) for external morphology and that of for genital morphology, except for the term endophallite (Génier 2019). The subgenus-level is avoided for this study since Phanaeus and Notiophanaeus have been proven to be artificial groups (Price 2007(Price , 2009Gillett & Toussaint 2020), and Notiophanaeus will probably be considered a synonym of Phanaeus in future works.…”