Nat Allia Vicente
email: natalliavicentte@gmail.com

Gael J Kergoat

Jiajia Dong

Karla Yotoko

Fr Ed Eric Legendre

Romain Nattier

Tony Robillard

In and out of the Neotropics: historical biogeography of Eneopterinae crickets

Keywords: ancestral area reconstruction, Bayesian relaxed clock, Boreotropical dispersal, crickets, disjunct distribution, dispersal-extinction-cladogenesis, fossil calibration, historical biogeography, Neotropics colonization

Aim Multiple biogeographical scenarios involving vicariance and different colonization routes can explain disjunct species distributions in the Southern Hemisphere. Here, we tested several alternative hypotheses in Eneopterinae crickets, a diverse subfamily presenting a disjunct worldwide distribution. We inferred a dated phylogeny of Eneopterinae and reconstructed their biogeographical history to unravel the origin of their present-day distribution, focusing on their multiple origins in the Neotropics.

Location Worldwide.

Methods We sampled 62 eneopterine species representing all extant genera. We inferred their phylogenetic relationships through Bayesian and maximum likelihood approaches based on four mitochondrial and three nuclear gene sequences. Divergence time estimates were inferred using Bayesian relaxed clock approaches and primary fossil calibrations. Biogeographical analyses were conducted with the default dispersal-extinction-cladogenesis (DEC) model and a variant model (DEC+J), which accounts for rare-jump dispersal events.

Results

Our dating analyses showed that the Eneopterinae is far older than expected and its diversification can be traced back to the Late Cretaceous (c. 76 Ma). In this context, the most supported biogeographical scenario (under DEC+J) suggests that the Neotropics were colonized twice independently: first during the break-up of Gondwana, when Antarctica, Australia and South America started separating (compatible with a vicariance event if relying on the result of the DEC model alone); later through a northern recolonization originating from Southeast Asia, likely related to a Holarctic Boreotropical distribution of an eneopterine lineage during the Eocene.

Main conclusions

We provided a dated worldwide biogeographical framework for the Eneopterinae crickets. Overall, the subfamily disjunct distribution pattern is better explained by both ancient and recent dispersal events. Whether this could reflect a widespread pattern in insect groups exhibiting a disjunct distribution remains to be investigated by studying other insect lineages. The information gathered here will also help foster new directions for future studies concerning the acoustic innovations of this clade.

diversity of their communication signals (e.g. [START_REF] Robillard | Mechanisms of high frequency song generation in brachypterous crickets and the role of ghost frequencies[END_REF][START_REF] Ter Hofstede | Evolution of a communication system by sensory exploitation of startle behavior[END_REF]. They exhibit a disjunct distribution throughout the tropics (Fig. 1), which makes them a suitable model for testing alternative routes of colonization of the Southern Hemisphere. For this group, a molecular phylogeny was developed during previous work to test whether the clades distributed in the region of New Caledonia were older than the emergence of the main island in this archipelago [START_REF] Nattier | Older than New Caledonia emergence? A molecular phylogenetic study of the Eneopterine crickets (Orthoptera: Grylloidea)[END_REF]. Although this study had a more regional focus, its results suggested multiple origins of theses insects in the Neotropics.

Here, we infer a new phylogeny of Eneopterinae by expanding the gene and taxonomic sampling. We calibrate the corresponding phylogeny according to a critical review of the fossils available for Grylloidea. Based on the resulting timetree, we perform biogeographical analyses to (1) investigate the hypothesis of multiple colonizations of South America by the Eneopterinae and (2) understand the origin of the extant disjunct distribution of the subfamily.

MATERIALS AND METHODS

Taxon sampling and molecular dataset

In this study, we sampled 62 Eneopterinae species representing all recognized genera, sequenced for three nuclear markers [histone H3 (H3), 18S and 28S ribosomal RNA] and four mitochondrial markers [cytochrome oxidase subunit I (COI), cytochrome b (Cytb), 12S and 16S ribosomal RNA]. In comparison with the most recent molecular phylogeny dealing with Eneopterinae [START_REF] Nattier | Older than New Caledonia emergence? A molecular phylogenetic study of the Eneopterine crickets (Orthoptera: Grylloidea)[END_REF], our study increased the sampling of genes and species for the subfamily (seven genes and 62 species versus four genes and 43 species).

For outgroup comparison, we used an approach based on the availability and quality of fossils in Grylloidea provided by the database 'Orthoptera Species File Online' [START_REF] Cigliano | Orthoptera Species File[END_REF]. We selected outgroup species from a recently published phylogeny of crickets [START_REF] Chintauan-Marquier | Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis[END_REF] containing molecular data for six of the markers we use (H3, 18S, 28S, Cytb, 12S and 16S). For each fossil species that was preselected for calibrating the molecular tree, we sampled two or three species of the corresponding clade in the cricket phylogeny. Using this strategy, we integrated 21 outgroup species encompassing Gryllidae, Gryllotalpidae, Mogoplistidae, Phalangopsidae, Trigoniididae, plus two Acrididae species (Caelifera) to serve as more external outgroups. A complete list of specimens, voucher taxa and GenBank accession numbers, are presented in Appendix S1 in Supporting Information.

INTRODUCTION

Explaining disjunct distributions among continents is a central goal in biogeography [START_REF] Lomolino | Biogeography[END_REF]. Major theories regarding biogeographical mechanisms have emerged from debates dealing with the relative importance and interplay of tectonic-driven vicariance resulting from the breakup of Gondwana and long-distance dispersal (LDD) [START_REF] Raven | Angiosperm biogeography and past continental movements[END_REF][START_REF] Waters | Molecular phylogenetics and biogeography of galaxiid fishes (Osteichthyes: Galaxiidae): dispersal, vicariance, and the position of Lepidogalaxias salamandroides[END_REF][START_REF] Heads | South Pacific biogeography, tectonic calibration, and pre-drift tectonics: cladogenesis in Abrotanella (Asteraceae)[END_REF]; but see [START_REF] Crisp | Hypothesis testing in biogeography[END_REF][START_REF] Gillespie | Long-distance dispersal: a framework for hypothesis testing[END_REF][START_REF] Waters | Biogeography off the tracks[END_REF]. Although dispersal and vicariance have been viewed as mutually exclusive, competing, hypotheses in the past, they are now seen as complementary mechanisms to understand the biogeographical history in widespread groups of organisms (e.g. [START_REF] Gamble | Coming to America: multiple origins of New World geckos[END_REF][START_REF] Kergoat | Disentangling dispersal and vicariance patterns in armyworms: evolution and historical biogeography of the pest genus Spodoptera (Lepidoptera: Noctuidae)[END_REF][START_REF] Condamine | Global biogeographic patterns of swallowtails' diversification resolve their use of alternative colonization routes in Northern and Southern hemispheres[END_REF][START_REF] Rota | The importance of long-distance dispersal and establishment events in small insects: historical biogeography of metalmark moths (Lepidoptera, Choreutidae)[END_REF].

The biogeographical history of the Southern Hemisphere involves either old vicariance events relative to the breakup of Gondwana, LDD among southern continents, or faunal exchanges with the Northern Hemisphere, either through range expansion or regular dispersion. Regarding South America, since the Cretaceous, four main colonization routes, either through dispersion or vicariance, have been hypothesized according to Sanmartın & Ronquist (2004) (Fig. 1). The first is the North America connection (NAC). North American and South American biota were connected at least twice in the past [START_REF] Hay | Alternative global Cretaceous paleogeography[END_REF][START_REF] Woodburne | The great American biotic interchange: dispersals, tectonics, climate, sea level and holding pens[END_REF]. The first connection started during the mid-Cretaceous [100 million years ago (Ma)] at the level of proto-Caribbean islands and remained until Eocene (49 Ma). The second connection started with the process of formation of the Isthmus of Panama during Miocene (15 Ma) [START_REF] Montes | Middle Miocene closure of the Central American seaway[END_REF]. Here, it is worth underlining that although the consensus hypothesis assumes that the closure of Panama Isthmus and faunal interchange begun 3.5 Ma, recent studies have also demonstrated substantial dispersal of terrestrial organisms much earlier [START_REF] Bacon | Species delimitation, patterns of diversification and historical biogeography of the Neotropical frog genus Adenomera (Anura, Leptodactylidae)[END_REF]. The second is the transatlantic route (TAC). Despite that Africa and South America separated completely around 100 Ma, transatlantic migration is the most supported colonization route for many animal groups in different time periods (e.g. [START_REF] Mayr | Out of Africa: fossils shed light on the origin of the hoatzin, an iconic Neotropic bird[END_REF][START_REF] Kergoat | Disentangling dispersal and vicariance patterns in armyworms: evolution and historical biogeography of the pest genus Spodoptera (Lepidoptera: Noctuidae)[END_REF][START_REF] Bond | Eocene primates of South America and African origins of New World monkeys[END_REF]. The third is the trans-Antarctic route (TAN). Antarctica connected Australia and South America from late Cretaceous (100.5 Ma) until Eocene (35 Ma), when the Southern Ocean between Tasmania and Antarctica opened. The fourth is the trans-Pacific route (TP). New Zealand separated from Gondwanan landmasses c. 80 Ma. However, the TP route is a likely explanation for disjunct distributions between South America and New Zealand sister-group taxa (e.g. [START_REF] Keogh | Molecular and morphological analysis of the critically endangered Fijian iguanas reveals cryptic diversity and a complex biogeographic history[END_REF][START_REF] Sharma | Out of the Neotropics: Late Cretaceous colonization of Australasia by American arthropods[END_REF][START_REF] Wei | Eurasian origin, boreotropical migration and transoceanic dispersal in the pantropical fern genus Diplazium (Athyriaceae)[END_REF].

In this work, we use the cricket subfamily Eneopterinae as a model system to test hypotheses that might explain diversification and distribution patterns in widespread biota. The c. 250 species of Eneopterinae (sensu Robillard & Desutter-Grandcolas, 2008) have been extensively studied for the anatolicus Sharov and the 122 Ma Brontogryllus excelsus Martins-Neto) have uncertain assignation since they rely on incomplete impressions of the tegmen. Therefore, we choose to implement a wide-outgroup approach to calibrate our dating analyses [START_REF] Sauquet | Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales)[END_REF][START_REF] Strijk | In and out of Madagascar: dispersal to peripheral islands, insular speciation and diversification of Indian ocean daisy trees (Asteraceae)[END_REF] based on fossils that, according to the descriptions, could be reliably addressed (for details about fossil choice, see Appendix S2). As result we set up a total of eight calibration procedures for the BRC analyses (UCLN versus RLC; two or four fossil constraints; uniform or exponential distributions). Four distinct relaxed clocks were specified based on the result of a PartitionFinder analysis (with beast option) (Appendix S3). For each calibration procedure, two runs were carried out with 50 million generations and trees sampled every 5000 generations. Based on the result, beast .xml files were modified to implement the path-sampling procedure for B F estimation following the recommendations of [START_REF] Baele | Accurate model selection of relaxed molecular clocks in Bayesian phylogenetics[END_REF]. We used a conservative burn-in period of 12.5 million generations per run. Post burn-in trees from the two runs (7500 trees for each run) were combined using LogCombiner. Convergence of runs was assessed graphically using the Tracer module of beast and by examining the effective sample size (ESS) of parameters. For all dating analyses, ESS ≥ 200 was obtained for all parameters. Out of the eight calibrations, the one relying on two fossil constraints, UCLN clocks and exponential distributions, has the best harmonic mean (À66,783.39) and is significantly recovered as the best-fit calibration procedure in all but one B F comparisons (Appendix S4). Additional analyses were also carried out using this calibration procedure (UCLN clocks and , 2006) with each gene separately to check for contaminations and artefacts. We concatenated sequences and used PartitionFinder 1.1.1 [START_REF] Lanfear | PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses[END_REF] with the Bayesian information criterion to infer the best partitioning schemes and substitution models [START_REF] Ripplinger | Does choice in model selection affect maximum likelihood analysis[END_REF]. For that, the coding genes were separated according to codon position. A combined ML tree was then obtained with RAxML using 100 replicates (support assessed using 1000 nonparametric BS replicates). A combined Bayesian inference (BI) analysis was carried out using MrBayes 3.2.3 [START_REF] Ronquist | MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space[END_REF]; eight Markov chains were run simultaneously for 50 million generations, sampled every 1000 generations to ensure independence of samples. We used a conservative burn-in of 12.5 million generations per run after checking for stability on the log-likelihood curves and the split-frequencies of the runs. Support of nodes for MrBayes analyses was provided by clade posterior probabilities (PP) as directly estimated from the majorityrule consensus topology. A clade with a PP value higher than 0.95 was considered as well supported.

Dating analyses

Bayesian relaxed clock (BCR) analyses were carried out with beast 1.8.3 [START_REF] Drummond | Bayesian phylogenetics with BEAUTi and the BEAST 1.7[END_REF] The separate analyses of each marker showed no major conflict of topology. On the combined dataset, BI (Appendix S7) and ML (Appendix S8) yielded largely congruent topologies, which recovered Eneopterinae as monophyletic with high support (BS: 95; PP: 1; Fig. 2). Except for Eneopterini, all the currently recognized tribes were retrieved as monophyletic and can be matched to supported clades in our analysis. The subfamily is separated in two main groups, one encompassing the Australian Eurepini (BS: 100; PP: 1) and the other including all remaining tribes: Eneoptera, one genus of the polyphyletic Eneopterini (BS: 100; PP: 1) as the sister group of the remaining tribes. The next clade gathered the two genera of Nisitrini (BS: 100; PP: 1), Paranisitra and Nisitrus as the sister group of the remaining Eneopterinae. Next, Xenogryllini, including Pseudolebinthus and Xenogryllus (BS: 100; PP: 1), appeared as a sister group of the species rich Lebinthini (BS: 88; PP: 1), including two genera previously classified as Eneopterini, Ligypterus and Ponca. Lebinthus is paraphyletic, as previously found. The other generic relationships were well defined, all genera being monophyletic.

Divergence time estimations

Both calibration procedures yielded comparable timeframes (Appendices S9-S16). Age estimates for Eneopterinae (Fig. 2, Table 1) suggested an origin 76.29 Ma [median age; 95% highest posterior density confidence interval (HPD): 63.28-96.76 for the best-fit calibration procedure]. See Table 1 for the details of molecular dating of the major clades of Eneopterinae. Regarding South America, our results showed that the lineage corresponding to Eneoptera branched during late Cretaceous at 70.97 Ma (95% HPD: 58.74-90.06 Ma), with a crown group diverging in early Miocene at 22.26 Ma (95% HPD: 16.25-30.66 Ma). The ancestor of the second Neotropical lineage (Ligypterus and Ponca) is dated at 40.17 Ma (95% HPD: 30.7-52.92 Ma), but Ligypterus began diversifying during the Miocene at 12.73 Ma (95% HPD: 9.29-17.35 Ma).

Historical biogeography

Model selections through LRT significantly supported the DEC+J model (L = À107.44) over the DEC model (L = À116.09) as the best-fit model for the 'BioGeoBears' historical biogeography analyses. The corresponding inference of ancestral areas evolution (Fig. 2) suggested an origin in Australia for Eneopterinae during the Late Cretaceous (76 Ma). Subsequently one lineage underwent diversification in Australia (Eurepini), whereas the second one colonized the Western Hemisphere via South America. An interesting pattern is then suggested, involving a subsequent colonization of the Old World (Southeast Asia) from the Western Hemisphere c. 70 Ma. This dispersal event was followed in the Palaeocene by a colonization of India. During the exponential distributions) in order to estimate the rates of evolution for each gene of our dataset (Appendix S5).

Historical biogeography

Historical biogeography analyses were carried out using the R package 'BioGeoBears' [START_REF] Matzke | Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades[END_REF]. This package relies on the Lagrange [START_REF] Ree | Maximum likelihood inference of geographic range evolution by dispersal, local extinction, and cladogenesis[END_REF]) DEC model. It also implements the model DEC+J that accounts for founder event speciation associated with rare-jump dispersal events [START_REF] Matzke | Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades[END_REF]. Here, we carried out separate analyses for the DEC and DEC+J models. As a guide tree, we used the dated phylogeny (single consensus tree inferred with LogCombiner) relying on corresponding to the best-fit calibration procedure (two fossil constraints, UCLN clocks and exponential distributions). This tree was further pruned to only include Eneopterinae in order to avoid potential biases resulting from the fact that outgroup taxa were sparsely sampled. We then defined 10 geographical areas after considering the evidence available for historical relationships between relevant geographical areas (Sanmartın et al., 2001;Sanmartın & Ronquist, 2004) and the distribution of Eneopterinae (Fig. 1). The biogeographical regions were Africa, Australia, Central America, India, New Caledonia, New Guinea, Palaearctic, northern South America, Southeast (SE) Asia and Southwest Pacific.

Following the views of several authors [START_REF] Hines | Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus)[END_REF][START_REF] Mansion | Phylogenetic analysis informed by geological history supports multiple, sequential invasions of the Mediterranean basin by the angiosperm family Araceae[END_REF][START_REF] Nylander | Accounting for phylogenetic uncertainty in biogeography: a Bayesian approach to dispersal-vicariance analysis of the trushes (Aves: Turdus)[END_REF], taxa with marginal distribution in an area were not assigned to it. Species ranges were coded by presence-absence and a maximum number of two areas were set for both DEC and DEC+J analyses. Finally, to account for major periods of geological rearrangements, we used time-stratified biogeographical models, with three time slices. The first time slice (t1) runs from 80.0 to 65.0 Ma, the second (t2) from 65.0 to 30.0 Ma and the last (t3) from 30.0 to 0.0 Ma. For each time slice, we provided a matrix of probabilities of dispersion (for details about palaeogeographical model, see Appendix S6), constructed according to the geographical connectivity between areas. To measure connectivity, we considered land bridges between the landmasses that could favour biotic exchange (e.g. Kerguelen Plateau). The rate of dispersion was scaled according to the availability of area connection through time. The factors were as follows (modified from [START_REF] Condamine | Global biogeographic patterns of swallowtails' diversification resolve their use of alternative colonization routes in Northern and Southern hemispheres[END_REF]:

(1) adjacent areas: 1.0; (2) areas separated by a minor barrier: 0.7; (3) dispersal between two areas separated by one area: 0.3; (4) LDD: 0.01; (5) dispersal impossible (one area missing): 0. After running both analyses, we used likelihood ratio tests (LRT) to sort between the two competing models (DEC and DEC+J).

RESULTS

Phylogenetic analyses

The complete molecular matrix comprised 3340 base pairs for 83 terminals. Appendix S3 shows the partition scheme of Oligocene, several lineages also reached New Guinea and the southwest Pacific from Southeast Asia. One lineage (now encompassing Ligypterus and Ponca) went back to the Western Hemisphere at the same period. Colonization of New Caledonia occurred more recently, but shortly after the reemergence of the Archipelago. Analyses with a DEC model also recovered a quite similar pattern (Appendix S17), noticeably differing by the fact that several vicariance events are inferred using the DEC model (especially at the base of the tree between Australia and South America), contrary to the result of the DEC+J analysis, which exclusively inferred dispersal events.

DISCUSSION

Phylogenetic and systematic account

This study presents the most complete molecular phylogeny of the globally distributed Eneopterinae. The new topology, including more taxa and based on more molecular markers, matches the topology of [START_REF] Nattier | Older than New Caledonia emergence? A molecular phylogenetic study of the Eneopterine crickets (Orthoptera: Grylloidea)[END_REF], including the polyphyly of the Neotropical tribe Eneopterini. The branch leading to the crown of Eneoptera diverged very early as the sister group of all other non-Australian Eneopterinae. The two other Neotropical genera, Ligypterus and Ponca, clustered within the tribe Lebinthini, which is corroborated by the acoustic characteristics shared by these clades [START_REF] Robillard | Bioacoustics of the Neotropical Eneopterinae (Orthoptera, Grylloidea, Gryllidae)[END_REF]. Ligypterus and Ponca are also morphologically similar to Lebinthini. The grouping of Eneopterini (Eneoptera, Ligypterus and Ponca) found earlier when only morphological data were used for phylogenetic reconstruction (Robillard & Desutter-Grandcolas, 2004a[START_REF] Stamatakis | RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models[END_REF] appears to be a reconstruction artefact due to weak synapomorphies about details of female wing venation and male genitalia. Therefore, the tribe Eneopterini should be restricted to the genus Eneoptera until further notice, while Ligypterus and Ponca are transferred to Lebinthini, as a Neotropical branch of this tribe (Fig. 2).

Our study positioned Pseudolebinthus as the sister genus of Xenogryllus, and Centuriarus and Gnominthus within Lebinthini. These genera were recently described and have not been included in a phylogeny. Centuriarus and Gnominthus form a clade located between the paraphyletic Lebinthus and the clade (Agnotecous, Pixibinthus), also found in [START_REF] Anso | Old lineage on an old island: Pixibinthus, a new cricket genus endemic to New Caledonia shed light on Gryllid diversification in a hotspot of biodiversity[END_REF]. The genus Swezwilderia, previously considered as Eneopterinae incertae sedis (Robillard & Desutter-Grandcolas, 2008), is confirmed within the tribe Lebinthini, as suggested by previous studies [START_REF] Nattier | Older than New Caledonia emergence? A molecular phylogenetic study of the Eneopterine crickets (Orthoptera: Grylloidea)[END_REF][START_REF] Chintauan-Marquier | Laying the foundations of evolutionary and systematic studies in crickets (Insecta, Orthoptera): a multilocus phylogenetic analysis[END_REF]. It seems related to the clade (Ligypterus+Ponca), although this relationship is poorly supported.

Historical biogeography of Eneopterinae

This study is the first attempt to reconstruct a biogeographical scenario for a clade of crickets with a worldwide distribution using modern phylogenetic methods for historical biogeography (Fig. 3a; Appendix S18). Dating analyses suggest that the radiation of Eneopterinae began in the late-mid Cretaceous about 76 Ma (Fig. 2) (95% HPD: 63-96 Ma). This result is much older than the 46 Ma found by the study by [START_REF] Nattier | Older than New Caledonia emergence? A molecular phylogenetic study of the Eneopterine crickets (Orthoptera: Grylloidea)[END_REF], which greatly underestimated the age of the clade by using recent geographical calibration points.

Our 'BioGeoBears' historical biogeography analyses suggest that the subfamily originated in Australia during the Late Cretaceous, which was still connected to Antarctica (Fig. 3a). Subsequently one lineage underwent diversification in Australia (Eurepini) (Fig. 3a, orange arrow), whereas the second one colonized South America through the trans-Antarctic route (Fig. 3b, green arrow: genus Eneoptera, nowadays distributed in the north of South America). This 'out-of-Australia pattern' through the TAN has been also inferred in other insect groups such as colletid bees [START_REF] Almeida | Biogeography and diversification of colletid bees (Hymenoptera: Colletidae): emerging patterns from the southern end of the world[END_REF] or fig wasps [START_REF] Cruaud | Out of Australia and back again: the world-wide historical biogeography of non-pollinating fig wasps (Hymenoptera: Sycophaginae)[END_REF]. In colletid bees, the initial diversification of Australian and South American lineages also occurred in the Late Cretaceous [START_REF] Almeida | Biogeography and diversification of colletid bees (Hymenoptera: Colletidae): emerging patterns from the southern end of the world[END_REF], when Antarctica, Australia and South America started breaking up (c. 90 Ma;[START_REF] Mcloughlin | The breakup history of Gondwana and its impact on pre-Cenozoic floristic provincialism[END_REF][START_REF] Sanmart In | Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns[END_REF]. As many as 14 trans-Antarctic interchanges were recovered between Australia and South America, suggesting a dynamic pattern in which vicariance events possibly had a pivotal role in explaining the current disjunct ranges of colletid bees [START_REF] Almeida | Biogeography and diversification of colletid bees (Hymenoptera: Colletidae): emerging patterns from the southern end of the world[END_REF]. As a word of caution, it is also worth highlighting that analyses with the DEC model alone inferred a basal vicariance event between Australia Table 1 The molecular dating (Ma) of major clades of Eneopterinae. HPD, highest posterior density. The information about clades distributed in South America is presented in grey. investigated in animal groups (but see [START_REF] Hines | Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: Apidae: Bombus)[END_REF][START_REF] Condamine | Global biogeographic patterns of swallowtails' diversification resolve their use of alternative colonization routes in Northern and Southern hemispheres[END_REF][START_REF] Van Damme | Tropical amphi-pacific disjunctions in the Cladocera (Crustacea: Branchiopoda)[END_REF], we suggest that this large green belt played a crucial role in Eneopterinae dispersion during Eocene as well.

In parallel, the dispersal of ancestral Swezwilderia from SE Asia towards islands of the southwest Pacific (Fiji, Samoa) (Fig. 3b; Appendix S18) was probably due to ocean drift, since these islands were not connected to landmasses and were formed only during the Late Eocene-Oligocene [START_REF] Neall | The age and origin of the Pacific islands: a geological overview[END_REF]. The biodiversity of islands that were not formed by the fragmentation of continental landmasses depends fundamentally on dispersal. According to [START_REF] Gillespie | Long-distance dispersal: a framework for hypothesis testing[END_REF], the major vectors for such LDD in the Pacific are wind, ocean drift and birds. It is likely that wind patterns, storms and oceanic drift may have played important roles in the dispersal of crickets through the Pacific region.

New Caledonia has a complex geological history [START_REF] Grandcolas | New Caledonia: a very old Darwinian island?[END_REF]. Together with New Zealand, it separated from the Gondwana block very early during the late Cretaceous c. 80 Ma (Sanmart ın [START_REF] Sanmart In | Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns[END_REF]. From the end of the Cretaceous to the mid-Cenozoic, New Caledonia however, under water, emerging only 37 Ma [START_REF] Grandcolas | New Caledonia: a very old Darwinian island?[END_REF][START_REF] Pillon | Time and tempo of diversification in the flora of New Caledonia[END_REF]. New Guinea was a source area of dispersal of crickets to New Caledonia, as also suggested for other groups (Sanmart ın [START_REF] Sanmart In | Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns[END_REF][START_REF] Pillon | Time and tempo of diversification in the flora of New Caledonia[END_REF][START_REF] Swenson | Sapotaceae biogeography supports New Caledonia being an old Darwinian island[END_REF]. Thus, the ancestor of the endemic Focus on events occurring during the Eocene: second colonization of South America from the boreotropics, colonization of New Caledonia through New Guinea and newly formed islands of Southwest Pacific and Southeast Asia. Coloured arrows according to the colonized area (colour coding as that in Fig. 2). Dotted arrows represent alternative scenarios as discussed in text. Palaeogeographical maps reconstructed from [START_REF] Blakey | Gondwana paleogeography from assembly to breakup -a 500 my odyssey[END_REF] available at http://cpgeosystems.com/globaltext2. html). [Colour figure can be viewed at wileyonlinelibrary.com] (i.e. +Antarctica) and South America, a hypothesis that should not be dismissed because the DEC+J model does not favour widespread ancestors contrary to the DEC model [START_REF] Matzke | Model selection in historical biogeography reveals that founder-event speciation is a crucial process in island clades[END_REF].

The Western Hemisphere (SE Asia, tribe Nisitrini) was, thereafter, colonized during Early Palaeocene (67 Ma), through a northern route of colonization (Fig. 1, North America connection), either through a trans-Atlantic pathway or through the Bering Strait (Fig. 3a, yellow arrows), even if the latter scenario is less likely, as suggested by Sanmartın et al. (2001). Our results suggest that the subsequent recolonization of South America by Eneopterinae during the Eocene (40 Ma), corresponding to the lineage (Ligypterus+ Ponca), could have followed the same northern route as the colonization of Asia from South America, but from east to west (Fig. 3b, green arrows). Considering that most of the Holarctic region had a tropical climate during this period [START_REF] Morley | Cretaceous and Tertiary climate change and the past distribution of megathermal rainforests[END_REF], both the colonization of SE Asia and later the recolonization of South America may have been greatly facilitated through the likely persistence of northern lineages in the Boreotropical region, which are now extinct. This second colonization event, thus, constitutes a case of parallel Boreotropical migration from north to south (Sanmartın et al., 2001). A large number of plant families support the Boreotropics hypothesis (see the review of [START_REF] Christenhusz | Biogeographical patterns of plants in the Neotropicsdispersal rather than plate tectonics is most explanatory[END_REF]. Although Boreotropical migration is rarely to forest expansions and contractions, isolating forestadapted species during the contraction periods (Fouquet et al., 2014). Both the northern Andean uplift and the mid-Miocene optimum could have markedly affected Eneopterarelated lineages.

Habitat fragmentation and exposure to new environments likely resulted in sister taxa occupying contrasting habitats [START_REF] Damasceno | Revisiting the vanishing refuge model of diversification[END_REF]. Within Eneoptera, E. gracilis, E. guyanensis and E. nigripedis occupy restricted forested areas, while E. surinamensis presents a wide distribution encompassing open habitats in the entire northern half of South America and part of Central America [START_REF] Robillard | A revision of Neotropical Eneopterinae crickets (Orthoptera, Grylloidea, Eneopteridae) with a phylogenetic discussion[END_REF]) (Fig. 1). The forest expansions and retractions induced by Andean uplift and the mid-Miocene climatic optimum probably exposed the species of Eneoptera to different habitat conditions, leading to the divergence of a clade adapted to open and secondary habitats.

The second colonization of South America by Eneopterinae occurred c. 48 Ma with the divergence of the clade [Swezwilderia (Ligypterus+Ponca)] from the rest of the Lebinthini. Once in South America, the divergence between Ligypterus and Ponca matches the uplift of Central Andes [START_REF] Hoorn | Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity[END_REF]. The beginning of the divergence within Ligypterus could also be a result of abrupt increase of temperature subsequent to the mid-Miocene climatic optimum (15 Ma), followed by a gradual cooling until 10 Ma [START_REF] Poulin | Evolutionary versus ecological success in Antarctic benthic invertebrates[END_REF]. Nowadays, this genus is mainly distributed in the southeastern coastal Brazil, but a few species and populations occur in the Amazon forest, in French Guiana and near Manaus, but remain largely unstudied in many locations.

CONCLUSION

In this study, we provided a worldwide-dated biogeographical model for the Eneopterinae crickets. Our results are congruent with general predictions proposed for the evolution of groups with disjunct distributions (Sanmart ın [START_REF] Sanmart In | Southern Hemisphere biogeography inferred by event-based models: plant versus animal patterns[END_REF]. However, the subsequent patterns, including a widespread distribution along Southeast Asia and Pacific Islands, do not fit with usual Gondwana-group distribution. Instead, it suggests that the current disjunct distribution of these crickets mostly results from dispersal, with a questionable early event that could correspond to either dispersal or vicariance according to the tested biogeographical model. Our results also indicate a Boreotropical dispersal route for Eneopterinae, corroborating suggestions that it was also a corridor for animals. High-frequency songs are a putative acoustic innovation in eneopterines (Robillard & Desutter-Grandcolas, 2004b), which have led to new modalities of communication [START_REF] Ter Hofstede | Evolution of a communication system by sensory exploitation of startle behavior[END_REF]. However, the initial circumstances that promoted their origin have been difficult to pinpoint given the lack of dated phylogenetic and biogeographical information. This study provides a first step towards when and where these acoustic innovations originated and will hopefully foster new directions for future multidisciplinary studies.

genera Agnotecous and Pixibinthus arrived in New Caledonia c. 31 Ma, diverging from the New Guinea lineage (Centuri-arus+Gnominthus) and giving rise to a highly diverse group both ecologically and acoustically [START_REF] Anso | Old lineage on an old island: Pixibinthus, a new cricket genus endemic to New Caledonia shed light on Gryllid diversification in a hotspot of biodiversity[END_REF].

To summarize, our study provides more statistical support to a scenario where South America was colonized twice through the TAN and NAC (Fig. 1), although a scenario with an initial vicariance is also possible. Extant eneopterines are not found in New Zealand, which is inconsistent with TP, while phylogenetic relationships between African and Neotropical lineages are inconsistent with TAC.

Multiple colonizations of Eneopterinae in South America but lack of diversity

According to the best-fit model (DEC+J), Eneopterinae colonized South America twice independently (Fig. 3). The early divergence of the lineage leading to extant representatives of Eneoptera (70 Ma) suggests a history of dispersal from Australia (Antarctica) to South America, through the Drake Passage. However, the hypothesis of an alternative vicariance event associated with a widespread ancestor could not be completely excluded here. Because this lineage now encompasses only a few species that are currently distributed in the northern part of South America, we postulate that this lineage has experienced several episodes of extinction in the past, as suggested by the long branch leading to the crown of the genus. Despite its rather old age, this lineage is poorly diversified compared with other Neotropical cricket lineages [START_REF] Robillard | A revision of Neotropical Eneopterinae crickets (Orthoptera, Grylloidea, Eneopteridae) with a phylogenetic discussion[END_REF]. The absence of this lineage in the southern part of South America could be explained by contraction of its distribution due to climatic factors, given that all extant eneopterines live in or near tropical rain forest. However, there is today no explanation of the marginal distribution of this lineage in Central America and its absence in the Caribbean. It is unlikely that the position of Eneoptera could be an artefact of long-branch attraction, as it is recovered both in ML and Bayesian analyses.

The northern Andean uplift (c. 23 Ma) marks the beginning of the divergence within Eneoptera. This geological event played an important role in the landscape and biota of northern part of South America, including Amazonia [START_REF] Hoorn | Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity[END_REF]. Subsequent influx of sediments into the Amazonian basin created different aquatic environments in the Amazonian landscape. In fact, the pollen records suggest the presence of rain forest combined with grasslands and/or floating meadows [START_REF] Hoorn | Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity[END_REF]. This new environment contributed to increase the local diversity, but the subsequent decline of wetlands isolated populations and resulted in diversification of aquatic invertebrates [START_REF] Wesselingh | Lake Pebas: a palaeoecological reconstruction of a Miocene, long-lived lake complex in western Amazonia[END_REF]), amphibians (Fouquet et al., 2014), mammals [START_REF] Matauschek | Mitochondrial phylogeny of tamarins (Saguinus, Hoffmannsegg 1807) with taxonomic and biogeographic implications for the S. nigricollis species group[END_REF] and reptiles [START_REF] Salas-Gismondi | A Miocene hyperdiverse crocodilian community reveals peculiar trophic dynamics in proto-Amazonian mega-wetlands[END_REF].

The mid-Miocene optimum (17-15 Ma) was an episode marked by a wet period followed by abrupt changes of temperature. These rapid environmental changes may have led

Figure 1

 1 Figure 1 Present-day distribution of Eneopterinae crickets showing the main hypothesized colonization routes towards South America (according to Sanmart ın & Ronquist, 2004); symbols: NAC, North America connection; TAC, Transatlantic route; TAN, Trans-Antarctic route; TP, Trans-Pacific route. The colours represent the distribution of the subfamily according to the 10 areas defined for the biogeographical analyses. [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 2

 2 Figure 2 Reconstruction of historical biogeography for Eneopterinae using a stratified dispersal-extinction-cladogenesis (DEC+J) model that accounts for geological history. The top-left box represents the 10 areas implemented in the palaeogeographical model. For each node, a coloured square corresponding to the coloured area in the box represents the inferred area(s) with the highest relative probability in the DEC+J analysis. Present-day distributions of each species are given at the tips by coloured circles corresponding to coloured areas on maps and current tribal assignations are mentioned on the right. The time slices of each palaeogeological period used to measure the dispersal rate are shown. A 5-Ma time scale is placed at the bottom of the chronogram spanning epochs since 90 Ma. Photo: male of Macrobinthus jharnae. Palaeogeographical maps reconstructed from Blakey (2008) available at http://cpgeosystems. com/globaltext2.html). [Colour figure can be viewed at wileyonlinelibrary.com]

Figure 3

 3 Figure3Biogeographical reconstruction for Eneopterinae. (a) Focus on events occurring in the late Cretaceous: divergence of two lineages, one colonizing Australia, the second colonizing the Western Hemisphere through South America. (b) Focus on events occurring during the Eocene: second colonization of South America from the boreotropics, colonization of New Caledonia through New Guinea and newly formed islands of Southwest Pacific and Southeast Asia. Coloured arrows according to the colonized area (colour coding as that in Fig.2). Dotted arrows represent alternative scenarios as discussed in text. Palaeogeographical maps reconstructed from[START_REF] Blakey | Gondwana paleogeography from assembly to breakup -a 500 my odyssey[END_REF] available at http://cpgeosystems.com/globaltext2. html). [Colour figure can be viewed at wileyonlinelibrary.com]

ACKNOWLEDGEMENTS

We thank both editors for their handling of the manuscript, and three anonymous referees for their comments and suggestions. We thank A. Nel for his help finding the documentation about fossils, L. Desutter-Grandcolas for her help selecting outgroup species and corresponding DNA sequences used in this study, F. de Assis Ganeo de Mello for providing some of the Neotropical samples, A. Gorochov for providing some of the Xenogryllini samples and A. Dehne Garcia for his help on the CBGP HPC computational facility. This research was partly funded by CNPq -Brazil, PROTAX [158726/2013-8] and CAPES; PDSE -[BEX 2609/14-2] and benefitted from financial support provided by CNPq and FAPEMIG, Process N. 563360/2010-0, Edital N. 47/2010, SIS-BIOTA Brazil. The laboratory work was carried in the Service de Syst ematique mol eculaire (SSM, UMS 2700 CNRS) of the MNHN: we thank M.C. Boisselier, C. Bonillo, D. Gey and J. Lambourdi ere for their help in data acquisition. This work was partly supported by agreement no. 2005/67 between the Genoscope (Evry, France) and the MNHN project 'Macrophylogeny of life'; sequencing was also undertaken in the project @SpeedID proposed by F-BoL, the French Barcode of life initiative and the network 'Biblioth eque du vivant' funded by the CNRS, INRA and MNHN. The laboratory procedures were partly realised through Action Transversale du Mus eum (ATM-MNHN) 'Biodiversit e actuelle et fossile' and ATM 'Barcode'. The samples from Papua New Guinea were obtained in the framework of 'Our Planet Reviewed Papua-New-Guinea 2012-2013' set up by Pro-Natura International, MNHN and IRD in partnership with the Royal Belgian Institute of Natural Sciences, the New Guinea Binatang Research Center, the University of Papua New Guinea, and the Divine Word University of Madang and with core funding of Prince Albert II of Monaco Foundation, the Stavros Niarchos Foundation, the Total Foundation, the Fondation d'entreprise EDF, the Fonds Pacifique, Spiecapag, Entrepose Contracting, the New Caledonia Government, the Reef Foundation and the Belgian National Lottery.

SUPPORTING INFORMATION

Additional Supporting Information may be found in the online version of this article:

DATA ACCESSIBILITY

All newly generated sequences were deposited in GenBank (Appendix S1).

Natallia Vicente is a research scientist interested in biodiversity distribution patterns, cryptic species and systematics.

Author contributions: N.V., T.R. initiated the study; N.V., T.R., G.J.K. designed the study; T.R. coordinated permits and collection sites; T.R., N.V., F.L. collected field samples; N.V., T.R., J.D., R.N. produced molecular data; N.V., T.R., J.D., G.J.K. analysed molecular data; N.V., T.R., K.Y. drafted the initial manuscript; N.V., T.R., K.Y., G.J.K., R.N., F.L. contributed to write the article.


Corentin Jouault
email: �jouaultc0@gmail.com

Frédéric Legendre
email: �frederic.legendre@mnhn.fr

Vincent Perrichot
email: �vincent.perrichot@univ-rennes1.fr

Fabien L Condamine
email: �fabien.condamine@gmail.com

André Nel

Redescription of Litholingia rhora Ren, 2002 (Neuroptera: Grammolingiidae) from the Middle Jurassic of Daohugou

Keywords: emended diagnosis, fossil record, Grammolingiidae, new specimen, taxonomy

whether they are published or not. The documents may come

Introduction

Within the insect order Neuroptera (lacewings), the superfamily Psychopsoidea (silky lacewings) is sister to the Myrmeleontoidea (antlions) and has an important fossil record with a series of extinct families extending from the Triassic to the Cretaceous [START_REF] Engel | Phylogeny and evolution of Neuropterida: Where have wings of lace taken us[END_REF] fig. 2). The family Grammolingiidae [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF] is one of the oldest psychopsoid families and was created to accommodate several fossil neuropterans from the Middle Jurassic of China [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF]. If most of the recent works on this family follow its placement within the Psychopsoidea, some authors rather suggested that the family Grammolingiidae belongs to the superfamily Osmyloidea (Makarkin et al., 2013: fig. 7; [START_REF] Yang | A new genus of the family Panfiloviidae (Insecta, Neuroptera) from the Middle Jurassic of China[END_REF]. Herein, we follow the placement of Grammolingiidae within the Psychopsoidea [START_REF] Engel | Phylogeny and evolution of Neuropterida: Where have wings of lace taken us[END_REF]. Currently, the family encompasses 21 species distributed in five genera (Table 1). This clade is, most of the time, treated as a family, but some authors also proposed a subfamily rank (= Grammolingiinae) within the Panfiloviidae [START_REF] Engel | Phylogeny and evolution of Neuropterida: Where have wings of lace taken us[END_REF]. However, as no phylogenetic analysis supports this placement, in the present work, we retain the family rank of the Grammolingiidae but remain aware that this status can change. The Grammolingiidae lack the vena triplica of the remaining Psychopsidae but share with other psychopsoid families a broadly constructed costal field. Here, we redescribe, using new material, one of the fossil species belonging to the Grammolingiidae, i.e., Litholingia rhora (initially described from Daohugou), whose type specimen did not permit the observation of specific parts of the wing, which is critical to separate species and define characters for future phylogenies.

Material and methods

The new specimen of Litholingia rhora originates from the Middle-Upper Jurassic deposit of Daohugou, Hiafanggou Formation, China. It was first treated as Bathonian-Callovian age [START_REF] Chen | Isotope geochronology of the fossil-bearing beds in the Daohugou area, Ningcheng, Inner Mongolia[END_REF] then the dating was refined and a Callovian-Oxfordian age was proposed [START_REF] Liu | U-Pb Zircon age for the Daohugou biota at Ningcheng of Inner Mongolia and comments on related issues[END_REF][START_REF] Liu | LA-ICPMS Zircon U-Pb dating in the Jurassic Daohugou beds and correlative strata in Ningcheng of Inner Mongolia[END_REF] and recent works suggest a late Middle Jurassic to early Late Jurassic age [START_REF] Huang | The Middle-Late Jurassic Yanliao entomofauna[END_REF][START_REF] Huang | Jurassic integrative stratigraphy and timescale of China[END_REF][START_REF] Lian | The early assemblage of Middle-Late Jurassic Yanliao biota: checklist, bibliography and statistical analysis of described taxa from the Daohugou beds and coeval deposits[END_REF]. Palaeoflora suggests a subtropical, warm temperate and humid climate [START_REF] Wang | Biodiversity and palaeoclimate of the Middle Jurassic floras from the Tiaojishan Formation in western Liaoning[END_REF]. The deposit was formed in the vicinity of an active volcanic area as evidenced by the presence of volcanic tuff levels resulting from periodic heavy ash Redescription of Litholingia rhora Ren, 2002 (Neuroptera: Grammolingiidae) from the Middle Jurassic of Daohugou rain; the landscape was covered with torrents and rivers as well as deep lakes [START_REF] Tan | New cupedids from the Middle Jurassic of Inner Mongolia, China (Coleoptera: Archostemata)[END_REF].

The specimen was examined using a Nikon SMZ25 stereomicroscope and photographed with a Nikon D800 camera. All images are digitally stacked photomicrographic composites of several individual focal planes, which were obtained using Helicon Focus. The figures and drawings were composed with Adobe Illustrator CC2019 and Photoshop CC2019 software. The specimen presented herein is housed in Nanjing Institute of Geology and Palaeontology, Chinese Academy of Science (NIGPAS), China under the accession number NIGP177501.

Wing venation nomenclature is modified from [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF] with additions from [START_REF] Schubnel | To be or not to be: postcubital vein in insects revealed by microtomography[END_REF].

Abbreviations are as follows: A = anal veins; CuA = cubitus anterior; CuP = cubitus posterior; MA = media anterior; MP = media posterior; PCu = post cubitus (= A1 for other authors, see detailed explanation in [START_REF] Schubnel | To be or not to be: postcubital vein in insects revealed by microtomography[END_REF]; RA = radius anterior; RP = radius posterior; ScP = subcostal posterior. Hind wing with a vein configuration similar to forewing, except for costal field with only one row of cells.

Systematic palaeontology

Litholinga rhora

Identification key to

Discussion

In the Grammolingiidae, the new specimen cannot be attributed to the genus Chorilingia owing to its second dichotomy of RP (= most proximal branch of Rs in [START_REF] Shi | Chorilingia (Neuroptera: Grammolingiidae): A new genus of lacewings with four species from the Middle Jurassic of Inner Mongolia, China[END_REF] not separating far from the first RP dichotomy (vs. separating far from the first RP dichotomy in Chorilingia). Additionally, the second dichotomy of RP is not distad the fork of CuA nor the fork of CuP while it is in Chorilingia (Shi et al., 2012: 2). Following the key to Grammolingiidae Ren, 2002 initially proposed by [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF], the new specimen cannot be placed in the genus Leptolingia because it possesses a forewing with 1A terminated on the posterior margin before the separation of the first branch of Rs from Rs [Here 1A is PCu and the first Rs branch corresponds to the second dichotomy of RP since [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF] considered the first RP dichotomy as MA]. Similarly, the new specimen cannot be attributed to the genus Grammolingia because CuA forks after CuP while CuA normally forks before CuP in Grammolingia [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF]. Khramov (2012: 298) proposed the following diagnosis for the genus Protolingia "Sc and R1 are fused in the distal part of wing and run by common stem to the wing margin". The condition of ScP and RA in the distal part of the wing is unknown in the new specimen but the different configuration of the costal field is sufficient to prevent attribution of the new specimen to the genus FIGURE 3. Wing venation patterns of Litholingia species with diagnostic vein characters highlighted in red and labelled (modified from [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF][START_REF] Shi | Two new fossil lacewing species from the Middle Jurassic of Inner Mongolia, China (Neuroptera: Grammolingiidae)[END_REF][START_REF] Khramov | The new fossil lacewings of Grammolingiidae (Neuroptera) from the Jurassic of Central Asia and Mongolia, with notes on biogeography of the family[END_REF].

Protolingia. However, due to the poor preservation of the holotype of Protolingia it is important to consider the genus with prudence. The genus Litholingia is defined using the following characters [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF]: Forewing PCu terminated on the posterior margin beyond the separation of the second branch of RP from RP; CuA forks after the fork of CuP; CuA and CuP forked beyond the second dichotomy RP [Note that PCu corresponds to A1, and RP to Rs in [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF]]. All these characters are present in the new specimen; therefore, we place it in the genus Litholingia. To date, there are only five species included in the genus Litholingia: L. eumorpha, L. longa, L. polychotoma, L. ptesa, L. rhora [START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF][START_REF] Shi | Two new fossil lacewing species from the Middle Jurassic of Inner Mongolia, China (Neuroptera: Grammolingiidae)[END_REF][START_REF] Khramov | The new fossil lacewings of Grammolingiidae (Neuroptera) from the Jurassic of Central Asia and Mongolia, with notes on biogeography of the family[END_REF]. Litholinga longa is difficult to compare with the new specimen due to the poor preservation of the type material (Khramov, 2012: figs 4, 5). In the original description, it is mentioned that "L. longa differs from other four species of Litholingia by the pectinate CuP" (Khramov, 2012: 302). The new specimen does not possess a similar configuration of the CuP preventing its attribution to the species L. longa. The new specimen can be rapidly separated from L. ptesa owing to its coloration pattern with small dark stripes or spots while L. ptesa possesses several broad black stripes on the forewings (Shi et al., 2011: fig. 4b). Additionally, it differs from L. ptesa in lacking a third RP branch forked near its base (vs. forked near it base in L. ptesa; Shi et al., 2011: fig. 4a). Since no branch of RP is forked near its base (= deeply), affinity with L. polychotoma is refuted, the latter having the fourth branch of RP deeply forked (Ren, 2002: figs 10, 11). L. eumorpha has a relatively simple CuP (i.e., with a reduced number of branches; Ren, 2002: figs 8, 9) while the new specimen possesses a CuP with five branches (i.e., heavily branched), and a coloration pattern of wings with large dark stripes (Ren, 2002: figs 8, 9) while the new specimen shows a relatively reduced coloration pattern with large white area. Therefore, it is clear the new specimen does not belong to the species L. eumorpha. The type species of the genus Litholingia (L. rhora) possess a similar wing venation with a CuP heavily branched and a distinctive coloration pattern nearly identical to that of the new specimen (Ren, 2002: figs 4-6). Since no character is found to separate the new specimen from L. rhora, we attribute it to this species. The new specimen described in this publication is helpful to document the branching pattern of MA and MP (see description part), which was not preserved in the holotype of the species. It also increases the number of occurrences of the species, these occurrences being essential for macroevolution analyses.

FIGURE 1 .

 1 FIGURE 1. Litholingia rhora Ren, 2002 Specimen NIGP177501. Habitus. Scale bar = 10 mm.

Order Neuroptera Linnaeus, 1758 Superfamily Psychopsoidea Handlirsch, 1906 Family Grammolingiidae Ren, 2002 Genus Litholingia Ren, 2002TABLE 1 .

 1 Diversity of the family Grammolingiidae Chorilingia euryptera Shi et al., 2012 China Callovian/Oxfordian Daohugou / Haifanggou Formation Shi et al., 2012 Chorilingia parvica Shi et al., 2012 China Callovian/Oxfordian Daohugou / Haifanggou Formation Shi et al., 2012 Litholingia rhora Ren, 2002 p. 57. Included species. Litholingia rhora Ren, 2002 (type species); other species: Litholingia eumorpha[START_REF] Ren | A new lacewing family (Neuroptera) from the Middle Jurassic of Inner Mongolia, China[END_REF], Litholingia longa Khramov, 2012, Litholingia polychotoma Ren, 2002, Litholingia ptesa Shi et al., 2011.

	Type species.
	Genus	Species	Distribution Period	Locality / Formation	Reference
	Chorilingia
		Chorilingia bakharica Khramov,	Mongolia	Bajocian/Bathonian	Bahar outcrop 208/4 / Togo-Khuduk	Khramov and
		2018			Formation	Vasilenko, 2018
		Chorilingia peregrina Shi et al., 2012 China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Shi et al., 2012
		Chorilingia translucida Shi et al.,	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Shi et al., 2012
		2012
	Grammolingia
		Grammolingia binervis Shi et al.,	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Shi et al., 2013
		2013
		Grammolingia boi Ren, 2002	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Ren, 2002
		Grammolingia sticta Shi et al., 2013 China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Shi et al., 2013
		Grammolingia uniserialis Shi et al.,	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Shi et al., 2013
		2013
	Leptolingia
		Leptolingia calonervis Shi et al., 2011 China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Shi et al., 2011
		Leptolingia imminuta Liu et al., 2011 China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Liu et al., 2011
		Leptolingia jurassica Ren, 2002	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Ren, 2002
		Leptolingia oblonga Khramov, 2012 Mongolia	Tithonian	Khoutiyn-Khotgor / Ulaan-Ereg	Khramov, 2012
					Formation
		Leptolingia shartegica Khramov,	Mongolia	Tithonian	Shar-Teg, outcrop 443/1 / Sharteg	Khramov, 2010
		2010			Formation
		Leptolingia tianyiensis Ren, 2002	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Ren, 2002
	Litholingia
		Litholingia eumorpha Ren, 2002	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Ren, 2002
		Litholingia longa Khramov, 2012	Kyrgyzstan Toarcian	Sai-Sagul, Shurab III / Sagul	Khramov, 2012
					Formation
		Litholingia polychotoma Ren, 2002	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Ren, 2002
		Litholingia ptesa Shi et al., 2011	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Shi et al., 2011
		Litholingia rhora Ren, 2002	China	Callovian/Oxfordian	Daohugou / Haifanggou Formation Ren, 2002
	Protolingia
		Protolingia mira Khramov, 2012	Kyrgyzstan Toarcian	Sai-Sagul, Shurab III / Sagul	Khramov, 2012
					Formation

Litholingia species

  , wings coloration pattern with thin dark stripes and broad white stripes...............Litholingia rhora -CuP pectinate or branched, if branched with less than five branches reaching wing margin, wings coloration pattern with broad dark stripes and thin white stripes.............................2 2. CuP pectinate............................................Litholingia longa -CuP with a variable number of branches but never pectinate.....................................................................................3 3. Fourth branch of RP deeply forked, three branches of CuA originating at its fork.....................Litholingia polychotoma -Fourth branch of RP forked far distad its origin, two branches of CuA originating at its fork..............................4 4.

	1.	CuP heavily branched (with five branches reaching
		wing margin)

Third branch of RP deeply forked, CuP likely with less than four branches, RP with seven branches.....................................................Litholingia ptesa -Third branch of RP forked far distad its origin, CuP with four branches, RP with at least nine branches............................................ Litholingia eumorpha

FIGURE 2. Litholingia rhora Ren, 2002 Specimen NIGP177501. Interpretative line drawing of fore-and hind wing venations with names of veins labelled, dotted lines represent hypothetical trajectory of veins not preserved (trichosors and coloration pattern omitted). Scale bar = 10 mm.

Acknowledgements

We are grateful to Prof. Dany Azar and an anonymous reviewer for their valuable comments. This work is part of the PhD. project of Corentin Jouault on the " Impact des interactions biotiques et paléo-évènements sur la diversification des insectes Neuropterida ".