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Molecular Phylogenetic Approach for Studying Life-History Evolution: the Ambiguous Example of the Genus Medicago L

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Molecular Phylogenetic Approach for Studying Life-History Evolution: the Ambiguous Example of the Genus Medicago L Molecular phylogenetic approach for studying life-history evolution: the ambiguous example of the genus Medicago L. Gilles Bena1,2,3*, Bernard Lejeune2, Jean-Marie Prosperi3 and Isabelle Olivieri1,3 1Institut des sciences de l'Evolution, Place Eugene Bataillon, Universite¨ Montpellier II, cc065, 34095 Montpellier cedex 05, France 2Insitut de Biotechnologie des Plantes, Universite¨ Paris-Sud, Baª timent 630, F-91405 Orsay Cedex, France 3Laboratoire de Ressources Ge¨ ne¨ tiques et d'Ame¨ lioration des Luzernes Me¨ diterrane¨ ennes, INRA Montpellier-Domaine de Melgueil, 34130 Mauguio, France We present a molecular phylogeny including most species of the genus Medicago L. (Fabaceae). Based on the consensus of the 48 most parsimonious trees, life-history and mating-system characters are mapped, and a putative history of the genus is suggested. The most parsimonious reconstruction suggests an ancestral annual and sel¢ng state, and recurrent evolution towards perenniality and outcrossing. Based on theore- tical predictions and classical hypotheses of the history of the genus, di¡erent assumptions about the ancestral state and di¡erent weighting schemes of evolution between the character states are made. Assuming an outcrossing, perennial ancestral state (partly supported by morphological features) does not fundamentally change the reconstruction. To meet theoretical expectations, various weighting schemes favouring evolution towards annuality and sel¢ng are applied. In£uence and validity of such weighting schemes are discussed with regard to other studies. Keywords: molecular phylogeny; life-history evolution; weighting schemes; Medicago The goal of the present paper is to examine how mating 1. INTRODUCTION system and life history may have evolved in a group of Several theoretical studies have addressed the evolution of related species. We chose to study the genus Medicago. This plant mating systems (e.g. Lande & Schemske 1985; appears particularly well suited for our goal; there are 55^ Uyenoyama 1986; Ronfort & Couvet 1995; Morgan & 61 species in the genus and most have been, at least partly, Schoen 1997) and the evolution of plant life histories studied with regard to mating system and life history (Stearns 1976; Fox 1992; Ronce & Olivieri 1997), whereas (Heyn 1963; Lesins & Lesins 1979; Small & Jomphe empirical studies have concentrated on characterizing 1988). This is most likely because Medicago sativa (alfalfa) plant mating systems (Schemske & Lande 1985; Barrett is an important crop species worldwide (Hanson et al. & Harder 1996, and references therein), studying the 1988). The following three issues will be addressed: consequences of inbreeding depression (Jarne & Charles- 1. Has sel¢ng in this genus evolved from outcrossing (as worth 1993), and measuring the cost of reproduction expected), and, if so, how many times? (Primack 1979). One general conclusion of such studies is 2. Has annuality in Medicago evolved from perenniality that evolution from outcrossing towards sel¢ng is more and, conversely, could perenniality have evolved from likely than the reverse (but see Ronfort & Couvet 1995), annuality? and that evolution towards annuality is easier in sel¢ng 3. Is there any evidence for the coevolution of a given life species than in outcrossing species (Charnov et al. 1981). history with a given mating system? One question that has been rarely addressed is the joint evolution of life-history tactics and mating systems To answer these questions, we built a molecular phylogeny (Olivieri et al. 1994; Zhang & Wang 1994). Although based on the combined sequences of the external (ETS) empirical investigations based on molecular phylogenetic and internal (ITS) transcribed spacer region of the reconstruction should be very useful and allow theoretical nuclear ribosomal DNA (Bena et al. 1998b). predictions to be tested, relatively few studies have yet been carried out (Weller et al. 1995; Barrett et al. 1996; Desfeux et al. 1996; Kohn et al. 1996; Schoen et al. 1997). 2. MATERIALS AND METHODS One reason could be that the mating system is not always (a) Study species well known in groups of species large enough to study such We included 44 of the 55 Medicago species described by Lesins coevolution, but small enough to construct a robust phylo- & Lesins (1979) plus three other species (M. rigiduloides, geny. M. sphaerocarpos and M. syriaca) described by Small (1990), Small et al. (1990) and Gillespie & McComb (1991). At least one species *Author for correspondence ([email protected]). from each of the nine sections de¢ned by Lesins & Lesins (1979) Proc. R. Soc. Lond. B (1998) 265, 1141^1151 1141 & 1998 The Royal Society Received 11 February 1998 Accepted 26 February 1998 1142 G. Bena and others Life-history evolution in Medicago Table 1. Description of species studied number of mating life populations speciesa systemb historyc studiedd accession origine herbariumf M. carstiensis Wulf Out. Per. 2 2595 Bot. Gard. Brussel U 2440 Ottawa Res. Stat. U M. cretacea M. Bieb. Out. Per. 2 2975 Museum Paris U 2739 Coll. Kerguelen U M. falcata L. Out. Per. 2 22382 Russia L 2362 Gatersleben U M. sativa L. Out. Per. 3 DZA059 Algeria L Gabes Tunisia L Cuf101 Cult. L M. glomerata Balbis Out. Per. 1 83001 France L M. cancellata M. Bieb. Out. Per. 2 2713 Gatersleben U 2731 Former USSR U M. pironae Visiani Out. Per. 2 2729 Yugoslavia U 2843 Yugoslavia U M. arborea L. Out. Per. 2 Helios Greece F Melagon Algeria F M. lupulina L. Sel. Per. 3 F20018 France L ES66 Spain L GR66 Greece L M. marina L. Sel. Per. 2 GR00X Greece L Carnon France L M. su¡ruticosa Ramond Sel. Per. 2 FR11008 France L 66003 France L M. hybrida Trautverr. Sel. Per. 1 2446 Coll. Kerguelen U M. secundi£ora Durieu Sel. Ann. 2 DZA311 Algeria L PI537238 France W M. orbicularis L. Sel. Ann. 2 ES009 Spain L ES041 Spain L M. radiata L. Sel. Ann. 1 2589 Spain U M. heyniana Greuter Sel. Ann. 1 12027 Greece A M. rotata Boissier Sel. Ann. 2 SA14095 ? A IC350 ? I M. bonarotiana Arcangeli Sel. Ann. 2 2591 ? U 115216 Israel A M. noeana Boissier Sel. Ann. 2 early Iraq 15487 Iran A M. shepardii Post Sel. Ann. 2 26682 Turkey A 16402 Turkey A M. rugosa Desrousseaux Sel. Ann. 1 GR026 Greece L M. scutellata L. Sel. Ann. 3 GR045 Greece L ES103 Spain L F34044 France L M. soleirolii Duby Sel. Ann. 2 8615 Tunisia A 1334 Malta A M. italica Miller Sel. Ann. 3 ES050 Spain L Murray. Cult. A Torna¢eld Cult. A M. littoralis Rodhe Sel. Ann. 1 ES167 Spain L M. truncatula Gaertn Sel. Ann. 3 Jemalong Cult. A DZA246 Algeria L DZA201 Algeria L M. rigiduloides Small Sel. Ann. 3 IC632 Iraq I IC716 Iraq I 128275 Iraq A M. rigidula L. Sel. Ann. 2 ES024 Spain L ES016 Spain L M. murex Willd. Sel. Ann. 3 FR83009 France L DZA042 Algeria L 23199 Greece A M. sphaerocarpos Bertol Sel. Ann. 2 127474 Greece A 131585 Romania A (Continued) Proc. R. Soc. Lond. B (1998) Life-history evolution in Medicago G. Bena and others 1143 Table 1. (Continued) number of mating life populations speciesa systemb historyc studiedd accession origine herbariumf M. constricta Durieu Sel. Ann. 3 117743 Syria A 116288 Malta A GR068 Greece L M. turbinata L. Sel. Ann. 2 GR020 Greece L GR035 Greece L M. doliata Carmign. Sel. Ann. 2 ES047 Spain L DZA231 Algeria L M. sauvagei Ne© gre Sel. Ann. 1 11476 Morocco A M. laciniata L. Sel. Ann. 1 DZA239 Algeria L M. minima L. Sel. Ann. 1 DZA013 Algeria L M. praecox de Candolle Sel. Ann. 2 GR042 Greece L F20059 France L M. coronata L. Sel. Ann. 1 GR062 Greece L M. syriaca Small Sel. Ann. 2 124962 Turkey A 128437 Syria A M. polymorpha L. Sel. Ann. 3 ES103 Spain L CircleV. Cult. A F34003 France L M. arabica L. Sel. Ann. 2 ES057 Spain L GR067 Greece L M. disciformis de Candolle Sel. Ann. 1 GR023 Greece L M. tenoreana Seringe Sel. Ann. 1 4639 France A M. intertexta L. Sel. Ann. 1 DZA027 Algeria L M. ciliaris L. Sel. Ann. 1 ES101 Spain L M. muricoleptis Tineo Sel. Ann. 1 GR021 Greece L M. granadensis Willd. Sel. Ann. 1 2600 Coll. Lesins U Mel. o¤cinalis L. Out. Bia. 1 443 France L Mel. italica L. ? Ann. 1 FR0300 France L Trig. foenum-graecum L. Sel. Ann. 1 Nimes France L Trig. cretica L. ? Ann. 1 CR007 Crete L Trif. pratense L. Out. Per. 1 Alpilles France L Trif. subterraneum L. Sel. Ann. 1 Argeles France L a M., Medicago; Mel., Melilotus;Trig.,Trigonella;Trif.,Trifolium. Authorities are given according to Lesins & Lesins (1979), Small & Jomphe (1988), Small (1989,1990) and Gillespie & McComb (1991). b Out.outcrosser, Sel.selfer, ?unknown. c Per.perennial, Bia.biannual, Ann.annual. Life-history and mating-system characters were obtained from literature (Heyn 1963; Lesins & Lesins 1979; Small 1986b) and from personal observations. d One or two individuals per population included in the study were sequenced and analysed in the phylogenetic reconstruction, and at least two individuals per species. e Cult., cultivated varieties; Coll., collection. f L, Laboratoire de Ressources Ge¨ ne¨ tiques et d'Ame¨ lioration des Luzernes Me¨ diterrane¨ ennes (sampling byJ. M. Prosperi in natural popu- lations); A, Australian Medicago Genetic Resource Centre;W,Washington Regional Plant Introduction Station; U, Unite¨ d'Ame¨ lioration des Plantes Fourrage© res de Lusignan; F, Forest Institut Research of Thessalonique; I, International Centre for Agriculture Research in DryAreas. was included in the study. Thirty-¢ve of the 47 species studied (see Baldwin et al. (1995) for a review for the use of ITS in phylo- have been described as annual selfers, four as perennial selfers genetic reconstruction, and Bena et al.
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