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37 Cristian Román Palacios Department of Ecology And Bolet´ındel Museo de Entomolog´ıade la Universidad del Valle 17(2):37-46, 2017 37 ON THE DIVERGENCE OF PSOCIDAE (PSOCODEA, PSOCOMORPHA): FOSSILS OR BIOGEOGRAPHY? Cristian Rom´an Palacios Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721, U.S.A.; correo electr´onico: [email protected] Ranulfo Gonz´alez Obando Grupo de Investigaciones Entomolog´ıcas, Universidad del Valle, Cali-Colombia. Yherson Franchesco Molina Henao Departamento de Biolog´ıa,Universidad del Valle, Calle 13 No. 100-00, Cali, Valle, Colombia Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cam- bridge, Massachusetts 02138, U. S. A. RESUMEN Con m´asde 900 especies v´alidas,Psocidae es la familia m´asdiversa de psocodeos. A pesar de la que la informaci´onmolecular disponible ha permitido hipotetizar sobre las relaciones filogen´eticas entre los diferentes linajes, el contexto temporal ha sido hasta ahora poco discutido, y la influencia de factores intr´ınsecosy extr´ınsecosen su diversificaci´ones aun desconocido. En este art´ıculo probamos la congruencia de tres evidencias de divergencia (i.e. dos f´osilesy una biogeogr´afica),y discutimos la correlaci´onentre la edad de los clados y otros mayores eventos (e.g. geol´ogicos,ecol´ogicos).Encontramos que la familia Psocidae probablemente divergi´odurante la transici´onMesozoico-Paleozoico. Adem´as, las subsecuentes ramificaciones se los sub-linajes mayores ocurri´oen un corto tiempo entre 68 y 77 My. Estas fechas tambi´encorresponden con los cambios de diversificaci´onen m´ultiples linajes de angiospermas y el incremento en la temperatura global. Palabras clave: Reloj molecular, Ps´ocidos,Biogeograf´ıa,Tiempo, F´osiles. ABSTRACT With more than 900 valid species, Psocidae is the most diverse family of psocodeans. Even though the availability of molecular has allowed hypothesizing on the phylogenetic relations for the different lineages, the evolutionary timing is still poorly discussed and the influence of intrinsic and extrinsic factors on their diversification is hitherto unknown. In this paper, we aim to test the temporal congruence of three evidences (i.e., two fossils and one biogeographical constraint), and discuss the correlation between clade’s age and other major events (e.g., geological, ecological). We found that family Psocidae likely diverged during the Mesozoic – Paleozoic transition. Moreover, the subsequent splits of the major sub-lineages occurred in a short time interval between 68 to 77 Mya. These dates also correspond to diversification shifts in multiple angiosperm lineages and the increase in global temperature. Key words: Molecular clock, Psocids, Biogeography, Timing, Fossils. INTRODUCTION than 900 species have been described in ca. 80 Genera (Yoshizawa & Johnson 2008). As consequence of the high species richness and Psocidae is the largest family within the pso- relative few studies restricted to specific lo- codean Suborder Psocomorpha. To date, more 38 Roman et al., On the divergence of Psocidae: fossils or biogeography? cations and/or scientific disciplines, there is et al. 2006). Protein coding genes were aligned still a lack of knowledge about their ethology, using MAFFT (Katoh & Standley 2013) with physiology, morphology, biogeography, natural default parameters. The applied algorithm va- history and evolution (Liu et al. 2013; Slifer & ried between loci depending on its biological Sekhon 1977). This family has several biologi- functions and number of taxa included (E-ins-i cal features that allows being considered as an for Wg and COI; L-ins-i applied to H3; G-ins-i interesting study group: (i) extensive within- used in ND5). Non-protein-coding genes (16s, and-among-species morphological variation, 18s, and 12s) were analyzed using webPRANK (ii) cosmopolitan distribution, (ii) elevated (L¨oytynoja & Goldman 2010) with default para- richness, among others (Yoshizawa 2004; Yos- meters and based on their secondary structure. hizawa et al. 2011). The monophyly of family Psocidae is suppor- ted by both morphological and molecular da- ABSOLUTE DATING ta (Johnson & Mockford 2003; Yoshizawa & Johnson 2008). Even though the higher-level relations have been discussed before, the tem- Molecular dating was performed using the poral context has not been discussed in deep. multi-coalescent approach implemented in Psocopterans appeared during the Permian- BEAST 2 (Bouckaert et al. 2014). This met- Carboniferous transition in the fossil record hod estimates the different genealogies inclu- ( 300 Mya). This suggests two aspects: (i) the ded in the species reconstruction tree taking occurrence of a shift in diversity during the late by into account the stochasticity and incon- Jurassic, and (ii) that this lineage reached its gruence between gene /species trees (Heled & maximum diversity during the Cenozoic Oligo- Drummond, 2010). BEAUTi 2.2.3 was used cene (Labandeira & Eble 2000). Paleontologi- to create the input file for BEAST runs. An cal information has indicated a general pattern uncorrelated molecular clock was set with a about the psocopteran diversity extrapolated lognormal distribution to model substitution from different fossil deposits (i.e., Lagerst¨atte). rates across branches in the tree. We selec- Yet, the family Psocidae has not been expli- ted a Birth-Death speciation process for tree citly analyzed. In particular, two major papers building that accounts for extinction and spe- have attempted to give a temporal framework ciation events. We constrained several nodes to the evolution of the Psocidae. Misof et al. across the phylogeny based on three shreds of (2014) set the minimum bound for the diver- evidence of divergence related to fossils (two) gence of Psocodea in 200 Mya, and Bess et and biogeography (one). The dating parame- al. (2014) published a molecular clock for the ters and an background information for each Hawaiian species of Ptycta (Psocinae: Ptycti- of the applied constraints are shown in Table 1. ni). In this paper, we intend to provide the first discussion on the evolutionary timing for We used two independent Markov chain Monte the family Psocidae based on two fossils and a Carlo (MCMC) that ran in the CIPRES por- single biogeographic evidence. tal (Miller et al. 2011). BEAGLE library was used for our analyses (Ayres et al. 2011). Each MATERIAL AND METHODS MCMC consisted of 50 million generations log- ged every 50,000 samples. Convergence was TAXON SAMPLING AND SEQUEN- assessed in Tracer 1.6 based on the estimated CE ALIGNMENT sample size (ESS >200) of the parameters of interest. Nodes with support values (pp) higher We sampled 120 species from 27 psocid genera. than 0.95 (Condamine et al. 2015) are consi- Outgroups were selected from families Myop- dered as well supported. Bayes factors were socidae, Psilopsocidae, and Hemipsocidae. We used for comparing the relative fit of the diffe- sampled four mitochondrial genes (12s, 16s, Cy- rent models (e.g. fossil 1, fossil 2 and biogeo- tochrome Oxidase subunit 1, and NADH dehy- graphy). Significant support of one hypothesis drogenase, subunit 5) and two nuclear genes concerning the other was confirmed by BF>5 (18s, and Histone 3; see Appendix 1; Benson (Condamine et al. 2015). Bolet´ındel Museo de Entomolog´ıade la Universidad del Valle 17(2):37-46, 2017 39 RESULTS and the Triassic (197 Mya; 129.22-262.95 Mya HPD), Amphigerontiinae 208 Mya (147.15- Molecular dating reconstructions indicated 274.21 Mya HPD) and finally Psocinae 293 congruent topologies despite the dating eviden- Mya (200.38-282.26 Mya HPD). ce. All the major lineages were recovered and highly supported (Fig. 1). However, discrepan- The three hypotheses of the Psocidae evolu- cies are clear when fossil- and biogeography- tionary timing suggest both ancient (F2 and based chronograms are compared. Both Fossil BG) and recent (F1) divergences. Compara- 2 (F2) and Biogeographic evidences (BG) in- tive analyses of relative fit of each model ap- dicated the older divergence of the lineage, proached from Bayes factors (Table 2), favored contradicting Fossil 1 (F1). Overall, the dif- biogeographic evidence (BF>5 for all pairwise ferent chronograms suggest that the family comparisons). This statistical support indica- divergence predates the Pangaea fragmenta- tes the biogeographic evidence is statistically, tion. a better explanation for the divergence of Pso- cidae than the dates recovered using F1 and Fossil dataset 1 (F1) sets the youngest diver- F2 evidence. gence times for all nodes in Psocidae. Moreover, this chronogram recovered the narrowest tem- DISCUSSION poral intervals across the tree (95 % HPD; i.e. low uncertainty and high confidence). This All analyses recovered the high-level phylogene- evidence places the divergence of the family tic relations proposed by Yoshizawa & Johnson during upper Cretaceous and Early Paleocene (2008). Our results suggest a pre-Pangaea di- (54 - 91 Mya). The crown ages of major lineages vergence of Psocidae in congruence with several occurred within 48 to 64 Mya. Kaindipsocinae ordinal-level dated phylogenies (Misof et al. is here the least derived and younger linea- 2014). The following discussion involves some ge (28.08-71.84 Mya HPD). The crown age remarks on different key aspects of the family of Amphigerontiinae and Psocinae may have evolutionary timing. occurred 61 and 64 Mya respectively (41.67- 80.81 Mya HPD; 49.38-79.44 Mya HPD). This evidence places the divergence of the major METHODOLOGICAL ARTIFACTS lineages of Psocidae during a recent and short AND FOSSILIZATION PROBABI- time interval. Fossil 2 (F2) suggests an ancient LITY divergence of the family. The crown age of Psocidae was placed during the Upper Jurassic Fossils described in Trichadenotecnum and Pso- (153.04 Mya; 152.02-155.02 Mya HPD) and the cidus (F1 evidence) may represent a substantial divergence of the major lineages in a narrow gap between the time of the cladogenetic events interval within 68.69-77.32 Mya. subfamily and their recovery. These fossils perhaps do not Kaindipsocinae (68.69 Mya) was recovered represent an accurate measure of the family as the youngest, followed by Psocinae (72.26 diversity and underestimate the divergence Mya) and Amphigerontiinae (77.32 Mya).
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