Cladistics Phylogenetic analysis of the diversification of the endemic cockroach Lauraesilpha in New Caledonia in relation to metalliferous soils and mountains For Peer Review Journal: Cladistics Manuscript ID: draft Manuscript Type: Article Date Submitted by the n/a Author: Complete List of Authors: Murienne, Jerome; Harvard University, Organismic and Evolutionary Biology; MNHN, Systematique et Evolution Pellens, Roseli; Museum national d'Histoire naturelle, Dpt Systematique et Evolution UMR 5202 Budinoff, Rebecca; American Museum of Natural History, Invertebrate Zoology Wheeler, Ward; American Museum of Natural History, Department of Invertebrates Grandcolas, Philippe; Museum national d'Histoire naturelle, Dpt Systematique et Evolution UMR 5202 Keywords: Endemism < Biogeography < Applications Cladistics Page 1 of 18 Cladistics 1 2 3 4 5 Phylogenetic analysis of the diversification of the endemic 6 7 cockroach Lauraesilpha in New Caledonia in relation to 8 9 metalliferous soils and mountains 10 11 12 13 Murienne J. a, b 14 Pellens, R. b 15 c 16 Budinoff, R. B. c 17 Wheeler, W. C. 18 For PeerGrandcolas, Review P. b 19 20 21 22 a- Harvard Universi ty, Departement of Organismic and Evolutionary Biology, 16 Divinity avenue 23 Biolabs 1119, Cambridge MA 02138 USA 24 b- UMR 5202 CNRS, Département Systématique et Évolution, case 50, Muséum national d’Histoire 25 naturelle, 45 rue Buffon, 75005 Paris, France 26 c- D ivision of Invertebrate Zoology, American Museum of Natural History, 79th Street at Central Park 27 28 West, New York, USA 29 30 31 Correspondence: Jérôme Murienne . E -mail: [email protected] 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Cladistics Cladistics Page 2 of 18 1 2 3 4 5 Abstract 6 7 New Caledonia is a tropical hot spot of biodiversity with high rates of regional and local endemism. 8 Even though it offers a great opportunity to study the evolution of endemism, it has received little 9 attention, particularly when compared to New Zealand , the nearest hotspot . Most studies on the 10 Neocaledonian en demism have been carried out at the regional level, contrasting groups and species 11 12 present in New Caledonia and absent in neighbouring territories. There is also evidence for remarkably 13 high local short -range endemism, mainly from plant studies, lizard and invertebrate taxonomy, and 14 mostly without a phylogenetic perspective. Most studies on endemism have referred to the geological 15 Gondwanan antiquity of the island and the stressing metalliferous soils derived from ultramafic rocks. 16 Very old clades are thoug ht to have been maintained in refugia and diversified on the metalliferous 17 soils. The present study is aimed at documenting the pattern of diversification and establishment of 18 For Peer Review 19 short range endemism in a phylogenetic context using the cockroach genus Lauraes ilpha . 20 Mitochondrial and nuclear genes were sequenced to reconstruct the phylogenetic relationships among 21 the species of this genus. The phylogenetic relationships and distribution of species did not support the 22 hypothesis of an origin with a radiation on metalliferous soils nor were consistent with areas of highest 23 rainfall . But Lauraesilpha species we re found to have similar altitudinal range and ecological habits 24 25 and to be short -range endemics on mountains . Closely related species were located on close o r 26 connected m ountains which probably played a role in the establishment of th is short -range endemism in 27 association with recent climatic change s. 28 29 Keywords: New Caledonia, endemism, phylogeny, cockroaches, ultramafic, mountains 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 Cladistics Page 3 of 18 Cladistics 1 2 3 4 5 6 Introduction 7 8 New Caledonia i s widely recognized as a biodiversity hotspot (Myers et al ., 2000). In addition to high 2 9 species richness for its small size (around 19000 km ), it shows an exceptional level of endemism. 10 Seventy -six percent of plant species (Lowry, 1998; Morat et al ., 2001 ), eighty -six percent of reptiles 11 (Bauer, 1999) , and up to hundred percent of many invertebrate groups (Holloway, 1979; Chazeau, 12 1993; Haase and Bouchet, 1998; Najt and Grandcolas, 2002) are endemic. This island also harbours a 13 14 large number of local short -range endemics restricted to small locations, either on peculiar soils or 15 mountains , but most of this short -range endemism has been only documented from plants studies and 16 taxonomic revisions of invertebrate groups. V ery few phylogenetic analyses have been undertaken to 17 understand the pattern and timing of diversification of these New Caledonian endemic biota (Good et 18 al ., 1997; Setoguchi et alFor., 1998; Pintaud Peer and Jaffré, Review 2001; Murienne et al ., 2005, Balke et al. 2006, 19 2007). Little is known about the origi n of these patterns of local endemism but several factors have 20 21 been invoked to explain them. The first factor is the soil diversity with especially the metalliferous 22 laterites derived from ultramafic rocks. New Caledonia was submerged and covered by the oc eanic 23 lithospheric mantle during Eocene and a terrane of ultramafic rocks developed on the whole Island at 24 this period (Clarke et al., 1997; Cluzel et al., 2001; Rawling and Lister, 2002; Crawford et al., 2004). 25 These rocks were later dissected by erosion and the pedogenesis gave birth to metalliferous and nickel - 26 27 rich soils (Paris, 1981; Crawford et al., 2004). These soils have been often mentioned as an adaptive 28 explanation for the occurrence of local endemism and richness in different groups of plants and animals 29 (Holloway, 1979; Haaese and Bouchet, 1998; Lowry, 1998; Pintaud and Jaffré, 2001 ; Bauer and 30 Sadlier, 2000 ). Distributional and phylogenetic patterns resulting from this adaptation to metalliferous 31 soils should typically substantiate radiations of species occurring on such soils with a smaller sister - 32 group occurring on other soils, as currently assumed for Araucaria trees (Setoguchi et al., 1998). A 33 34 second possible causal factor, the moutainous landscape and possibly its orogeny can also be invoked 35 in conjunction with temperature and rainfall , as done for New Zealand (Trewick et al ., 2000; Chinn and 36 Gemmell, 2004) . The new Caledonian orogeny is however much older than in New Zealand since it 37 dates back to the last major subduction events between 44 a nd 34 MY. New Caledonian landscape is 38 highly dissected with several distinct groups of mountains taking part of a complex central chain 39 40 culminating in several places at more than 1600m (Paris, 1981). As a matter of consequence, climatic 41 conditions vary a l ot according to elevation, western vs eastern slopes and other local particularities 42 (ORSTOM, 1981) . In this context, l ocal mountainous areas presently receiving the highest rainfall have 43 been seen as potential refuges for forest species during the driest period s of Pleistocene (Pintaud et al ., 44 2001). If mountains played a role in the establishment of short -range endemism, species should be 45 46 restricted to particular mountains and their phylogenetic relationships should portray the geographical 47 connections ex isting among the different parts of the central chain. If climatic conditions have been 48 more important in determing the endemism, a more strict relationship should be found between local 49 climate and species relationships, which could have diversified espec ially in highest rainfall areas for 50 forest species, not all mountainous areas. 51 52 In order to better understand the pattern of diversification of the New Caledonian biota, we studied one 53 local endemic radiation, the cockroach genus Lauraesilpha Grandcolas, 19 97 (Insecta: Blattidae , 54 Tryonicinae ). Cockroaches have already proved to be interesting groups for studying endemism in New 55 Zealand (Trewick, 2000; Chinn and Gemmell, 2004) and in New Caledonia (Pellens, 2004; Murienne et 56 al ., 2005) . Lauraesilpha cockroach es are small, flightless, wood -eating, and only found in New 57 58 59 60 Cladistics Cladistics Page 4 of 18 1 2 3 4 5 Caledonian rainforests (Grandcolas, 1997 ; Grandcolas et al., 2002 ). The number of Lauraesilpha 6 species occurring without sympatry on an island of only 400km long was remarkable when compared 7 to o ther tropical cockroach faunas where species have much larger distributions (Grandcolas, 1994; 8 Grandcolas and Pellens, 2006) but similar to previous observations on related genera in New Caledonia 9 (Pellens, 2004; Murienne et al., 2005). This situation perm its to study the diversification of the genus 10 Lauraesilpha as an example of Neocaledonian radiation with respect to metalliferous soils, mountains 11 12 and climate. The genus Lauraesilpha has been sampled in New Caledonia mainland and m itochondrial 13 and nuclear g enes have been sequenced in order to obtain a molecular phylogeny. The goal of this 14 phylogenetic study is to understand the pattern of diversification in the light of these three causality 15 factors. This will allow us to test (i) if an adaptive radiation of Lauraesilpha species occurred on 16 metalliferous soils, these species should then appear as a monophyletic group (ii) if species have 17 diversified in relation to mountains according to the shape of the landscape, species from the same 18 For Peer Review 19 mountain chain should t hen appear monophyletic independently of the substrate (iii) or mainly in 20 climatic areas of highest rainfall where species would appear monophyletic according to potential 21 refuges as hypothetised by Pinteaud & Jaffre (2001) . 22 23 24 Materials and methods 25 26 Sampling 27 28 The Lauraesilpha genus is distributed all over the New Caledonia mainland (Grande Terre) and several 29 species we re already found to be short -range endemics , but locally abundant where dead wood was in 30 31 sufficient quantity for their xylophagous habits (Grandc olas et al ., 2002).