Fleas (Siphonaptera) are Cretaceous, and Evolved with Theria

Abstract

Fleas (order Siphonaptera) are highly-specialized, diverse blood-feeding ectoparasites of mammals and birds with an enigmatic evolutionary history and obscure origin. We here present a molecular phylogenetic study based on a comprehensive taxon sampling of 259 flea taxa, representing 16 of the 18 extant families of this order. A Bayesian phylogenetic tree with strong nodal support was recovered, consisting of seven sequentially derived lineages with Macropsyllidae as the earliest divergence, followed by Stephanocircidae. Divergence times of flea lineages were estimated based on fossil records and host specific associations to bats (Chiroptera), suggesting that the common ancestor of extant Siphonaptera diversified during the Cretaceous. However, most of the intraordinal divergence into extant lineages took place after the K-Pg boundary. Ancestral states of host association and biogeographical distribution were reconstructed, suggesting with high likelihood that fleas originated in the southern continents (Gondwana) and migrated from South America to their extant distributions in a relatively short time frame. Theria (placental mammals and marsupials) represent the most likely ancestral host group of extant Siphonaptera, with marsupials occupying a more important role than previously assumed. Major extant flea families evolved in connection to post K-Pg diversification of Placentalia. The association of fleas with monotremes and birds is likely due to later secondary host association. These results suggest caution in casually interpreting recently discovered Mesozoic fossil "dinosaur fleas" of Northeast Asia as part of what we currently consider Siphonaptera.

Phylogenetic and compositional diversity are governed by different rules: a study of fleas parasitic on small mammals in four biogeographic realms

“…We constructed phylogenetic trees for fleas for each realm using the most recent molecular phylogeny (Zhu et al 2015) as the backbone. This tree presented data on 205 species and 110 genera.…”

“…This comprised almost all genera (but not all species) from our dataset. The positions of species not represented in Zhu's et al (2015) tree were determined according either to their morphologically derived taxonomic affinities (see Krasnov et al 2011 andHadfield et al 2014 for details) or additional molecular and/or morphological phylogenetic studies (Duchemin 2003, Lu and Wu 2003, Acosta and Morrone 2005.…”

“…We expected the effects of evolutionary processes to be stronger in the realms of the southern hemisphere and the effects of ecological processes to be stronger in the realms of the northern hemisphere. The former expectation is because fleas most likely have Gondwanan origin , Whiting et al 2008, Zhu et al 2015. As a result, the flea fauna of the Afrotropics and the Neotropics is represented by multiple species of the most basal lineages (Pulicidae and Stephanocircidae), whereas the youngest lineages (Leptopsyllidae and Ceratopsyllidae) are the most species-rich in the Nearctic and the Palearctic.…”

Fossils of parasites: what can the fossil record tell us about the evolution of parasitism?

“…Furthermore, a recent analysis by Zhu et al (2015) suggests a much later origin for Siphonaptera in the Early Cretaceous, well after the appearance of the 'giant fleas' described by Gao et al (2013) and Huang et al (2012Huang et al ( , 2013a, and that the ancestral hosts of the early fleas were therian mammals, with birds colonised later through a series of host-switch events (in agreement with the results of Whiting et al, 2008). Thus it remains questionable whether the 'giant fleas' were fleas at all, or if they belonged to a separate group of ectoparasitic insects that evolved and diversified during the Mesozoic to parasitise dinosaurs and/or pterosaurs, but became extinct during the Cretaceous-Paleogene extinction event 66 million years ago along with their hosts.…”

Progress, pitfalls and parallel universes: a history of insect phylogenetics

“…Given their almost unimaginable diversity, it is impossible for any individual to be considered an expert for all Hexapoda, and most workers spend their careers exploring particular groups. Here we list a sample of the recent advances from various authors in the phylogeny of Odonata [283 -290,292], Ephemeroptera [278,293,294], Plecoptera [295], Dermaptera [296], Embioptera [297], Phasmatodea [298], Dictyoptera [236,279,[299][300][301], Mantodea [302], Orthoptera [234,303 -306], Hemiptera [307,308], Psocodea [309], Hymenoptera [310 -317], Neuropterida [318 -320], Coleoptera [321 -323], Diptera [324,325], Lepidoptera [326 -334], Trichoptera [335 -337], Mecoptera [246,338,339] and Siphonaptera [340,341].…”