The Earliest Case of Extreme Sexual Display with Exaggerated Male Organs by Two Middle Jurassic Mecopterans Qi Wang, Chungkun Shih, Dong Ren* Key Lab of Insect Evolution and Environmental Change, College of Life Sciences, Capital Normal University, Beijing, China Abstract Background: Many extant male animals exhibit exaggerated body parts for display, defense or offence in sexual selection, such as male birds of paradise showing off colorful and elegant feathers and male moose and reindeers bearing large structured antlers. For insects, male rhinoceros and stag beetles have huge horn-like structure for fighting and competition and some male Leptopanorpa scorpionflies have very long abdominal terminal segments for sexual display and competition. Fossil records of insects having exaggerated body parts for sexual display are fairly rare. One example is two male holcorpids with elongate abdominal segments from sixth (A6) to eighth (A8) and enlarged male genitalia from Eocene, suggesting evolution of these characters occurred fairly late. Principal Findings: We document two mecopterans with exaggerated male body parts from the late Middle Jurassic Jiulongshan Formation in northeastern China. Both have extremely extended abdominal segments from A6 to A8 and enlarged genitalia, which might have been used for sexual display and, to less extent, for fighting with other males in the competition for mates. Although Fortiholcorpa paradoxa gen. et sp. nov. and Miriholcorpa forcipata gen. et sp. nov. seem to have affinities with Holcorpidae, we deem both as Family Incertae sedis mainly due to significant differences in branching pattern of Media (M) veins and relative length of A8 for F. paradoxa, and indiscernible preservation of 5-branched M veins in hind wing for M. forcipata. Conclusions/Significance: These two new taxa have extended the records of exaggerated male body parts of mecopterans for sexual display and/or selection from the Early Eocene to the late Middle Jurassic. The similar character present in some Leptopanorpa of Panorpidae suggests that the sexual display and/or sexual selection due to extremely elongated male abdominal and sexual organs outweigh the negative impact of bulky body and poor mobility in the evolutionary process. Citation: Wang Q, Shih C, Ren D (2013) The Earliest Case of Extreme Sexual Display with Exaggerated Male Organs by Two Middle Jurassic Mecopterans. PLoS ONE 8(8): e71378. doi:10.1371/journal.pone.0071378 Editor: David Carrier, University of Utah, United States of America Received January 22, 2013; Accepted June 27, 2013; Published August 14, 2013 Copyright: ß 2013 Wang et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research is supported by the National Basic Research Program of China (973 Program) (grant 2012CB821906), the National Natural Science Foundation of China (grants 31071964, 31172143, 31230065 and 41272006), PHR Project of the Beijing Municipal Commission of Education (grants 201207120), and China Geological Survey (grant 1212011120116). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction [5] who provided a description distinguishing and defining the family as required by article 13 of the International Code of Holcorpidae is an enigmatic and controversial extinct family in Zoological Nomenclature [6] for family names published after Mecoptera, which has been documented and debated since 1878. 1930. In 2010, Archibald distinguished Holcorpa from all known Scudder placed Holcorpa in the family Panorpidae in 1878, because Panorpidae by a combination of diagnostic characters: (1) fore-, he considered that the scorpionfly was closely related to Panorpa and hind wing media veins with five branches; (2) abdominal Linnaeus, 1758 [1]. Since then, the discovery of more fossil segments 6 (A6) to 8 (A8) elongate (both male, female), with A8 specimens with 5-branched M (Media) veins in both the fore- and distinctly longest; (3) male: extended, slender dististyli, lacking hind wings (vs. four-branched M veins in all Panorpidae) indicates basal tooth [7]. the genus Holcorpa Scudder, 1878 does not belong to Panorpidae. Fossil records of the Holcorpidae are fairly rare. Up to date, Carpenter [2] considered it has closest affinities with Old World only one fossil genus Holcorpa with two species Holcorpa maculosa genera, as its body structure is similar to Neopanorpa and Scudder, 1878 and Holcorpa dillhoffi Archibald, 2010 within this Leptopanorpa (Panorpidae), both of which are restricted to the Old family have been described. The first holotype specimen, H. World. Penny [3] and Martynova [4] suggested it should be placed maculosa, was described by Scudder [1]. The body is poorly into a separate family. Over years, many authors have subscribed preserved, incomplete beyond the eighth abdominal segment. The to the view of not considering Holcorpa as a panorpid, and have second specimen (allotype) was collected in 1907, which was mentioned the name ‘‘Holcorpidae’’ in some cases. It is Willmann identified as a male by Carpenter. The abdomen of the allotype is PLOS ONE | www.plosone.org 1 August 2013 | Volume 8 | Issue 8 | e71378 Extreme Sexual Display by Jurassic Mecopterans well preserved: the male genitalia clearly visible, with distinctive Nomenclatural Acts enlarged genital bulb and extended pincer-like gonostyli. Both The electronic edition of this article conforms to the require- fossils are from the Late Eocene of Florissant, Colorado, USA. ments of the amended International Code of Zoological Nomen- The other species is H. dillhoffi from the Ypresian (Early Eocene) clature, and hence the new names contained herein are available McAbee beds of British Columbia, Canada [7]. under the Code from the electronic edition of this article. This Compared to the holotype, the larger size of the allotype was published work and the nomenclatural acts it contains have been explained by Carpenter [2] as sexual dimorphism by concluding registered in Zoobank, the online registration system for the that the holotype is a female, contrary to Scudder’s opinion [1,7]. ICZN. The Zoobank LSIDs (Life Science Identifiers) can be Based on new data and information from new fossil material of [7] resolved and the associated information viewed through any and this study, we believe that the holotype should be considered standard web browser by appending the LSID to the prefix as sex indeterminate due to lack of preserved terminalia. The ‘‘Http://zoobank.org’’. The ISID for this publication is: urn:lsid:- sudden narrowing of A8, comparing with A7, is consistent with zoobank.org:pub:B2F83E59-492E-4B6C-81B8-59D501B4C301. male specimens in [7] and this study. The electronic edition of this work was published in a journal with Two new mecopterans, Miriholcorpa forcipata gen. et sp. nov. and an ISSN, and has been archived and is available from the Fortiholcorpa paradoxa gen. et sp. nov., are described herein. These following digital repositories: PubMed Central and LOCKSS. specimens were collected from the Jiulongshan Formation at Daohugou Village of Ningcheng County in Inner Mongolia, Results China [8–11]. Based on M with five branches in both fore- and hind wings; sixth to eighth abdominal segments exceedingly Systematic Palaeontology elongate and genitalia enlarged, F. paradoxa gen. et sp. nov. seems Mecoptera Packard, 1886 to have affinities with Holcorpidae. But, we deem F. paradoxa gen. Family Incertae sedis. et sp. nov. as Family Incertae sedis mainly due to significant Miriholcorpa Wang, Shih & Ren gen. nov. differences in branching pattern of Media (M) veins in hind wings; urn:lsid:zoobank.org:act:79F6D4BF-0D0C-4E02-88EE- length of A8 slightly longer than that of A7 (vs. A8 distinctively 660F7E5651D5 longest); and lacking spurs at the terminal part of A6 (vs. two spurs Type species. Miriholcorpa forcipata Wang, Shih & Ren sp. present). We also deem M. forcipata gen. et sp. nov. as Family nov. Incertae sedis, due to uncertainty whether its hind wing has 5- Etymology. The generic name is a compound word derived branched M veins. from a Latin word Miri-, meaning amazing, referring to the fact The age of the Daohugou fossil-bearing beds is considered to be that the specimen is amazingly and beautifully preserved and the late Middle Jurassic [12–14], ca. 165 Ma, corresponding to the Holcorpa, the type genus of Holcorpidae. Callovian–Bathonian boundary using a standard international Diagnosis. In forewing, Sc reaching anterior margin almost time scale [15]. Daohugou fossil-bearing beds contain abundant at middle of pterostigma. Rs furcation at same level as M. Stem of exquisite Mecoptera fossils. Until now, many specimens of Rs3+4 short. Stem of Rs1+2 1.5 to 2.0 times as long as stem of Pseudopolycentropodidae [16–18], Mesopsychidae [16,19], Eo- Rs3+4.M1 simple. M2+3 forking to M2 and M3,M4+5 forking to M4 meropidae [20], Bittacidae [21], Aneuretopsychidae [16,22,23] and M5. Only one crossvein between Cu1 and Cu2 (cu1-cu2). and Cimbrophlebiidae [21,24] have been reported from this Remarks. This genus has many diagnostic characters of locality. Holcorpidae such as forewing R1 curving around pterostigma, meeting C on anterior