Molecular Phylogeny And Biogeography Of Panorpoidea And Integrative Taxonomy Of Dicerapanorpa(Mecoptera)

The extant Panorpoidea(Insecta: Mecoptera)consists of Panorpidae and Panorpodidae.Panorpidae is the most speciose family in Mecoptera with approximately 470 described species in eight genera.Panorpidae is widely distributed throughout Asia,North America and Europe.To date,only a few phylogenetic studies on Panorpidae have been conducted with limited samples,and the internal relationships of Panorpidae remains unclear.Besides,little is known about the origin,dispersal and biogeographical process that resulted in the current distribution.This study based on molecular data explored the phylogenetic relationship,origin,and biogeographic history of Panorpidae.The species-poor family Panorpodidae consists of only 13 species in two genera,Panorpodes MacLachlan,1875 and Brachypanorpa Carpenter,1931.Panorpodes is distributed in eastern Asia and western North America,while Brachypanorpa is restricted to both weastern and eastern North America.Besides,fossil record of Panorpodes from Baltic amber suggests that the family occurred in Europe during the Priabonian.Based on historical biogeographical analysis,this study resolved the family's origins and revealed how the disjunct distribution of Panorpodidae in the Holarctic region were established.Dicerapanorpa Zhong & Hua,2013 is a small genus in Panorpidae,with only eight described species.The genus is distributed in the Qinling-Bashan and Hengduan mountains,a famous biodiversity hotspot in the world.Dicerapanorpa is divided into two groups,D.magna group and D.diceras group.Due to marked intraspecific morphological variation and interspecific similarity,the species of Dicerapanorpa are difficult to delimit and delineate.Based on the integrative taxonomic analysis,we explored the species delimitation of Dicerapanorpa.Besides,the unique distribution pattern,in combination with limited dispersal ability and habitat preference of Dicerapanorpa makes it an ideal model to investigate the mechanism of speciation and diversification of montane insects in eastern Asia.The main results are as follows:1)Molecular phylogeny and biogeography of Panorpidae: Based on three gene fragments,COI,COII and 28 S rRNA,we reconstructed the phylogeny and ancestral distribution area of Panorpidae.The phylogenetic analysis revealed that Sinopanorpa,Dicerapanorpa,and Cerapanorpa are all monophyletic groups,while Panorpa is paraphyletic with Sinopanorpa,Furcatopanorpa,Dicerapanorpa,and Cerapanorpa.The biogeographic reconstruction indicated that Panorpidae originated in eastern Asia during the period from early Paleogene to middle Eocene,and migrated eastward to North America through Bering land bridge and westward to Europe;Chinese Panorpidae dispersed to Japan,and was isolated from Japanese species due to the opening of Japanese sea.2)Historical biogeography of Panorpodidae: Based on the combined data of COI,COII,28 S rRNA and EF-1?,this study reconstructed the phylogeny of Panorpopidae,and confirmed the monophyly of both Panorpodes and Brachypanorpa.We also reconstructed the ancestral distribution range based on dispersal-vicariance analysis(DIVA),dispersal-extinction-cladogenesis(DEC),and Bayesian binary MCMC(BBM),and revealed that the initial diversification of Panorpodidae occurred during the Ypresian(53.9 Ma).A wide ancestral distribution in eastern Asia and western North America was inferred for Panorpodidae from the biogeographical analyses.The original range of Panorpodes across eastern Asia and western North America was fragmented by intercontinental vicariance after the submergence of Bering land bridge.The genus Brachypanorpa was initially restricted to western North America and subsequently dispersed into eastern region of North America.3)Integrative taxonomy of Dicerapanorpa: Based on the integrative analyses of DNA barcoding,morphological characters,geometric morphometrics,and molecular phylogeny,we discovered 12 new species(7 were published),raising the species number to 20.Thses new species are D.macula Hu,Wang & Hua,2019,D.deqenensis Hu,Wang & Hua,2019,D.tanae Hu,Wang & Hua,2019,D.tenuis Hu,Wang & Hua,2019,D.zhongdianensis Hu,Wang & Hua,2019,D.yijunae Hu & Hua,2019,D.luojishana Hu & Hua,2019,D.lativalva sp.n.,D.minshana sp.n.,D.hualongshana sp.n,D.zhengkuni sp.n.and D.bifurcata sp.n.The possible reasons of the paraphyly of several species of Dicerapanorpa might be incomplete lineage sorting,hybridization introgression,recent divergence etc.4)Causes of current distribution pattern of Dicerapanorpa: This study explored the biogeographical history and the causes of current distribution pattern of Dicerapanorpa based on four gene fragments,COI,COII,cytb,and 28 S rRNA.The result revealed that: Dicerapanorpa is a monophyletic group with four clades I–IV,and the divergence times within clade I–IV were estimated in the late Miocene(11.7,11.6,12.5 and 6.1 Ma,respectively),probably associated with the orogenic uplift of QTP;this genus has an origin in southern Hengduan and Bashan Mountains in the early Miocene(20.4 Ma);the ancestral populations in southern Hengduan Mountains expanded its range eastward into Guizhou Plateau and northward into Minshan Mountain through jump dispersal at cladogenesis events;the ancestral populations in Bashan Mountain migrated northward to Qinling Mountains and westward to Minshan Mountain;Dicerapanorpa was estimated to have a mean speciation rate of 0.143 species/Ma,extinction rate of 0.070 species/Ma,and diversification rate of 0.073 species/Ma.5)Evolutionary history of the D.magna complex: The D.magna complex consists of D.magna,D.minshana sp.n.,and D.hualongshana sp.n.Based on mtDNA COI,we analyzed the population genetics,and explored the evolutionary history and the influence of Pleistocene glaciation on speciation and divergence of the D.magna complex.The results showed that: the D.magna complex consists of three geographically structured lineages(I–III)dating back to Pleistocene,corresponding well with the Minshan,Bashan and Qinling Mountains;the overall genetic diversity were higher in Bashan than those in Qinling and Minshan,and Liping with highest genetic diversity might be a hybrid zone of secondary contact;lineage I–III experienced slight population increase or stability,long-term population stability followed by slight contraction,and population expansion in Pleistocene,respectively;the suitable habitats for the D.magna complex were Qinling and Bashan Mountains under both LGM and current conditions;the three lineages might be in a process of incipient speciation,and likely derived their current distribution from separate glacial origins,followed by vicariance and divergence.