New Mitochondrial and Nuclear Evidences Support Recent Demographic Expansion and an Atypical Phylogeographic Pattern in the Spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae)

Abstract

Philaenus spumarius is a widespread insect species in the Holarctic region. Here, by focusing on the mtDNA gene COI but also using the COII and Cyt b genes and the nuclear gene EF-1α, we tried to explain how and when its current biogeographic pattern evolved by providing time estimates of the main demographic and evolutionary events and investigating its colonization patterns in and out of Eurasia. Evidence of recent divergence and expansion events at less than 0.5 Ma ago indicate that climate fluctuations in the Mid-Late Pleistocene were important in shaping the current phylogeographic pattern of the species. Data support a first split and differentiation of P. spumarius into two main mitochondrial lineages: the “western”, in the Mediterranean region and the “eastern”, in Anatolia/Caucasus. It also supports a following differentiation of the “western” lineage into two sub-lineages: the “western-Mediterranean”, in Iberia and the “eastern-Mediterranean” in the Balkans. The recent pattern seems to result from postglacial range expansion from Iberia and Caucasus/Anatolia, thus not following one of the four common paradigms. Unexpected patterns of recent gene-flow events between Mediterranean peninsulas, a close relationship between Iberia and North Africa, as well as high levels of genetic diversity being maintained in northern Europe were found. The mitochondrial pattern does not exactly match to the nuclear pattern suggesting that the current biogeographic pattern of P. spumarius may be the result of both secondary admixture and incomplete lineage sorting. The hypothesis of recent colonization of North America from both western and northern Europe is corroborated by our data and probably resulted from accidental human translocations. A probable British origin for the populations of the Azores and New Zealand was revealed, however, for the Azores the distribution of populations in high altitude native forests is somewhat puzzling and may imply a natural colonization of the archipelago.

High genetic diversity in southwest Asian populations ofPhilaenus spumarius(Hemiptera: Auchenorrhyncha)

“…According to the results of this study and previous phylogenetic and phylogeographic works on this species (Maryańska-Nadachowska et al, 2010Seabra et al, 2010;Rodrigues et al, 2014), we can conclude that southwestern Asia is probably the place of origin of the Philaenus spumarius, or at least the main refugium for P. spumarius during the Pleistocene glaciations, from where this species spread across almost the whole Holarctic. Yet the history of this species is probably more complex, as several highly distinct subclades (known from the western and eastern Mediterranean, Crimea, the Caucasus, and Eastern Asia) need a long period of time to gain such divergence.…”

“…We also found a single population in northeastern Turkey with a haplotype closest to the NE clade, however forming a substantially highly distinct phylogenetic entity. It is important to highlight that previous studies (Maryańska-Nadachowska et al, 2012;Rodrigues et al, 2014) also identified highly distinct mitochondrial clades in the Caucasus (Georgia), Crimea, and Northern Anatolia (thus, around the Black Sea). However, in all of these regions were found phylogenetic lineages different from those found in this study in Turkey and Iran.…”

“…The discovery of new species in Southwestern Asia (Abdul-Nour & Lahoud, 1996;Tishechkin, 2013) and distinct clades within P. spumarius (Maryańska-Nadachowska et al, 2012;Rodrigues et al 2014) suggest that this area could shelter other evolutionary, or even taxonomic, units. In the present study, the genetic affinity of Turkish and Iranian populations of P. spumarius was studied.…”

Assessing genotype-phenotype associations in three dorsal colour morphs in the meadow spittlebug Philaenus spumarius (L.) (Hemiptera: Aphrophoridae) using genomic and transcriptomic resources

“…It is the most investigated species of its genus and has high genetic and morphological variation [29]. Sixteen adult colour phenotypes are known to occur in natural populations [30] but only 13 are referred in the literature.…”

Subterranean termite phylogeography reveals multiple postglacial colonization events in southwestern Europe

“…2006; Rodrigues et al. 2014). They also suggest that the key to understanding the origin of the R. grassei / R. banyulensis complex may lie in North African populations.…”