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. 2015 Feb 17;115(5):733–745. doi: 10.1093/aob/mcv001

A molecular survey concerning the origin of Cyperus esculentus (Cyperaceae, Poales): two sides of the same coin (weed vs. crop)

Olga De Castro 1,*, Roberta Gargiulo 1, Emanuele Del Guacchio 2, Paolo Caputo 1, Paolo De Luca 1
PMCID: PMC4373285  PMID: 25694438

Abstract

Background and Aims Cyperus esculentus is widespread in tropical and temperate zones and is also present in cooler regions. It is used as a crop plant, but it also occurs in the wild and as a weed. As a consequence of its ecological plasticity, C. esculentus has remarkable variability, with several morphotypes. Four wild-type varieties are presently recognized, in addition to the cultivated form. This study investigates the phylogenetic position and biogeography of C. esculentus with the objective of contributing new data to increase the understanding of its evolutionary history.

Methods Genealogical relationships among genotypes were inferred by using plastid DNA haplotype and nuclear ribosomal (nr) DNA ribotype sequences for 70 specimens either collected in the field or obtained from herbaria. Statistical dispersal–vicariance (S-DIVA) and Bayesian binary method (BBM) analyses were used to reconstruct the possible ancestral ranges of C. esculentus. In order to determine the age of C. esculentus, a time-measured phylogenetic analysis was performed.

Key Results Considerable variation between the chosen nuclear and plastid markers was detected (27 ribotypes vs. six haplotypes). No geographical structure was displayed among the haplotypes, but information on the dispersal pattern may be deduced. Two types of ribotypes were detected in nrDNA, with an evident geographical segregation into an Old World group and a polymorphic New World group. Both S-DIVA and BBM analyses suggested a biogeographical history in which dispersal from the African region has been crucial in shaping the current distribution pattern of C. esculentus. The most recent common ancestor between C. esculentus races has an age of 5.1 million years (95 % highest posterior density 2.5–10.2).

Conclusions The molecular analysis provides novel insights into the evolutionary history of C. esculentus. The results have various taxonomic and phylogenetic implications, including a hypothesis on the origin and phylogeography of this species, which probably originated in the late Cenozoic in Africa, and reached the Americas repeatedly, independently of Columbian exchanges.

Keywords: Chufa, Cyperus esculentus, Cyperaceae, crop, dispersal–vicariance analysis, herbarium specimens, long-distance dispersal, molecular clock, Poales, tiger nut, yellow nutsedge, weed

INTRODUCTION

Cyperus esculentus L. (yellow nutsedge or tiger nut), a perennial C4 plant of the sedge family (Cyperaceae), is widespread in tropical and temperate zones and is also present in cooler regions (Mulligan and Junkins, 1976; Holm et al., 1977; Wills, 1987; Milczak et al., 2001; Defelice, 2002; Larridon et al., 2011). It is a crop, but it also grows wild, very often as a weed (Holm et al., 1977; De Vries, 1991; Bryson and Carter, 2008). Cyperus esculentus presents a serious worldwide problem for agriculture because it is one of the most invasive plants known (Holm et al., 1977; Schippers et al., 1993; Halvorson and Guertin, 2003; Heidarzade and Esmaeili, 2013). Cyperus esculentus is an obligate outcrosser (Tayyar et al., 2003); its base chromosome number n is 54 or 108 (e.g. Hicks, 1929; Federov, 1969; Rath and Patnaik, 1978; Roalson, 2008) and no hybrids are known in nature according to Mulligan and Junkins (1976), although Tayyar et al. (2003) recognized a possible hybridization with C. rotundus L. The plant produces abundant seeds (Stoller and Sweet, 1987), but strong vegetative propagation through rhizomes and tubers is much more important than seeds in the diffusion of the species (Mulligan and Junkins, 1976; Rotteveel et al., 1993; Schippers et al., 1993; Halvorson and Guertin, 2003). The tubers are also a source of food for several animals (birds and mammals) (Mitchel and Martin, 1986; Schroeder and Wolken, 1989; ter Borg et al., 1998). To date, the long-distance dispersal of C. esculentus appears to be related to a large extent to human activities (i.e. as a contaminant in crop seeds), as reported by Mulligan and Junkins (1976) and ter Borg et al. (1998).

Cyperus esculentus is a sub-cosmopolitan weed, tolerating cold temperatures, but being more common in warmer zones (Holm et al., 1977). It grows on several substrates and in numerous, usually not too dry habitats, including fields and human-controlled environments (Mulligan and Junkis, 1976; Defelice, 2002). As a consequence of its ecological plasticity and wide distribution, C. esculentus is remarkably variable, with several morphotypes; this variability is exhibited as numerous specific and infraspecific taxa (Böckeler, 1870; Clarke, 1884; Britton, 1886; Ascherson and Graebner, 1902–1904; Kukenthal, 1935; ter Borg et al., 1988).

According to a complete morphometric analysis performed by Schippers et al. (1995), that was not accepted by Govaerts et al. (2014), four varieties of the wild type are currently recognized: C. esculentus var. esculentus, var. heermannii (Buckley) Britton, var. leptostachyus Boeckeler and var. macrostachyus Boeckeler. These four varieties have definite geographical origin and distributions. Cyperus esculentus var. esculentus is considered as a native of the Old Word (OW) and is widespread in southern Europe, Africa and Asia (Schippers et al., 1995). Information about its recent introduction to northern America has not yet been recorded in the Flora of North America (eFloras FNA; http://www.efloras.org/). Cyperus esculentus var. heermannii is the most geographically restricted, having only been reported in the southern USA (Schippers et al., 1995; eFloras FNA). This variety was introduced to the Netherlands in about 1970 according to ter Borg and Schippers (1992). Cyperus esculentus var. leptostachyus is most common in northern America and also occurs in southern America (Schippers et al., 1995; eFloras FNA). This variety has also been recorded in Europe since 1947 (ter Borg and Schippers, 1992). According to Guillerm (1987), C. esculentus var. leptostachyus was taken to France in 1947 and has diffused throughout Europe, because it is well adapted to cold climates and to agriculture (i.e. it is tolerant of herbicides). Finally, C. esculentus var. macrostachys is common from Central America to the southern USA (Schippers et al., 1995; eFloras FNA). It was accidentally introduced into the province of Zeeland (the Netherlands) in about 1972, together with Gladiolus cormlings (De Vries, 1991; ter Borg and Schippers, 1992).

The origin of the cultivated type (C. esculentus var. sativus Boeckeler) was located in the Mediterranean area, where it has been cultivated for its edible tubers since pre-dynastic Egypt (fourth millennium BC) (Schweinfurth, 1883; Serrallach, 1927; Negbi, 1992; Fahmy et al., 2014). At present, it is still cultivated for food and medicinal use in southern Europe, Africa and Asia (Holm et al., 1977; Zanotti, 1987; De Vries, 1991; Pascual et al., 2000; Arafat et al., 2009; Bamishaiye and Bamishaiye, 2011; Pascual-Seva et al., 2013). This plant was introduced to the USA as a potential vegetable crop by the US patent office in 1854 (Defelice, 2002). It is important to note that C. esculentus var. sativus is also regarded as a cultivar of var. esculentus (i.e. chufa) (Shilenko et al., 1979; Defelice, 2002; Arafat et al., 2009; Pascual-Seva et al., 2013). This cultivar status was officially proposed by De Vries in 1991, although it is not accepted by Govaerts et al. (2014).

In this study, we investigate the phylogenetic position and biogeography of C. esculentus with the objective of contributing new data to increase our understanding of the evolutionary history of this invasive species. Our lateral goal is to understand possible relationships among its varieties. To address these goals, we employed the novel sequencing of molecular markers and data sets as published by Christin et al. (2008) and Larridon et al. (2013). The molecular regions chosen for this study are located both in biparental nuclear DNA [nuclear ribosomal DNA (nrDNA)] and in uniparental plastid DNA. The plastid genome of most Poales is maternally inherited, reflecting gene flow by seeds (Harris and Ingram, 1991); the chosen molecular regions include two genes (rbcL and nadhF) and one intron (rps16), which have already been employed in Cyperus and C4 phylogenies (Muasya et al., 2002; Christin et al., 2008). In the nuclear genome, the chosen sequence, which was a variable fragment of the external transcribed spacer 1 (ETS1f), has already been used to study phylogenetics of C3 and C4 Cyperus (Larridon et al., 2011, 2013; Bauters et al., 2014).

MATERIALS AND METHODS

Plant material, taxonomic treatment and DNA extraction

Seventy specimens of Cyperus esculentus were collected in the field or obtained from the herbaria BM, K, LSU, MJG, NAP, PAL, RBGE, RNG and US. Varietal identification was performed according to Schippers et al. (1995). The accessions, vouchers and locality information are listed in Table 1. A geographical map of the specimens is shown in Fig. 1.

Table 1.

A list of Cyperus esculentus accessions used in the molecular study with variety names (det. = author of the identification at the varietal level), voucher information, origin and corresponding cpDNA haplotypes (rps16) and nrDNA ribotypes (ETS1f)

Code Cyperus esculentus varieties (det.) Origin (date) Voucher (Herbarium) rps16 No. ETS1f
OLD WORLD
Africa OW1 esculentus (Del Guacchio & Iavarone, 2012) Botswana, Ngamiland (11.03.1987) 199, Long et al. (RBGE) G1 O3
OW2 esculentus (Schippers, 1994) Ethiopia, Adua (08.1863) 21, Schimper (BM – 001118241) G1 O2
OW3 esculentus (Del Guacchio & Iavarone, 2012) Ethiopia, Ganale River (17.04.1974) 2416, Ash (US – 2819970) A2 O4
OW4 esculentus (Del Guacchio & Iavarone, 2012) Senegal, Dakar (09.09.1994) 17109, Laegaard (US – 3325063) A1 O2
OW5 esculentus (Del Guacchio & Iavarone, 2012) Somalia, Afgoi (19.09.1959) 2618, Moggi, Bavazzano (FI) G1 O2
OW6 esculentus (Del Guacchio & Iavarone, 2012) South Africa, Mosdene (22.5.1967) SA21 (MJG) G1 O2
OW7 esculentus (Del Guacchio & Iavarone, 2012) St. Helena Island (18.12.2007) T07-0280, Gremmen (RBGE) G3 O3
OW8 esculentus (Schippers, 1994) Tanzania, Mt. Kilimangiaro (04.1894) 2111, Volkens (BM – 1118239) G1 O1
OW9 esculentus (Schippers, 1994) Zimbabwe, Guampa Forest (01.1956) 17280, Goldsmith (BM – 1118236) G1 O2
OW10 esculentus (Del Guacchio & Iavarone, 2012) Zimbabwe, Lake Kyle (27.12.1990) 15906, Laegaard (US – 3261129) G3 O2
OW11† sativus Boeckeler Burkina Faso, Banfora (2009) B2, Billi (NAP) A1 O1
OW12† sativus Ghana (2009) B5, De Castro (NAP) A1 O1
OW13† sativus Nigeria (2010) B6, De Castro (NAP) A1 O1
Asia OW14 esculentus (Schippers, 1994) Georgia (1838) s.n., Hohenacker (BM – 1118251) G1 O2
OW15 esculentus (Schippers, 1994) Georgia, Lenkoran Jun. (1836) 2187, Hohenacker (BM – 1118252) G1 O5
OW16 esculentus (Schippers, 1994 India, Dehradun (06.1882) 2460, Duthie (BM – 1118246) G1 O5
OW17 esculentus (Schippers, 1994) India, Muttinadu (06.1892) 1294, Hohenacker (BM – 1118245) G1 O2
OW18 esculentus (Schippers, 1994) Turkey (1931) 911, Gorz (BM – 1118250) G1 O5
OW19 esculentus (Del Guacchio & Iavarone, 2012) Turkey, Rize 2376, Jenkins (RBGE) G1 O2
Europe OW20 esculentus (Del Guacchio & Iavarone, 2012) Azores Islands (21.05.1981) s.n., Wallace (RNG) G3 O2
OW21 esculentus (Del Guacchio & Iavarone, 2012) Ischia Island, Casamicciola (22.09.96) R6, Vallariello (NAP) A1 O1
OW22 esculentus (Del Guacchio & Iavarone, 2012) Pontine Islands, Ponza (23.09.1967) R1, Vallariello (NAP) G3 O4
OW23 esculentus (Del Guacchio & Iavarone, 2012) Pontine Islands, Ponza (08.05.2001) R2, Vallariello (NAP) G3 O2
OW24 esculentus (Del Guacchio & Iavarone, 2012) Sicily, Messina 48681, PAL G3 O2
OW25 esculentus (Del Guacchio & Iavarone, 2012) Sicily, Palermo 48927, PAL G1 O2
OW26 esculentus (Del Guacchio, 2010) Southern Italy, Bagnoli (03.2010) E1, Del Guacchio (NAP) A1 O2
OW27 esculentus (Del Guacchio, 2010) Southern Italy, Moschiano (09.2010) E3, Del Guacchio (NAP) A1 O2
OW28 esculentus (Del Guacchio, 2010) Southern Italy, Pontecagnano (09.2010) E2, Del Guacchio (NAP) A2 O2
OW29 esculentus (Del Guacchio & Iavarone, 2012) Spain, Cambrils (27.09.2003) 5539, Verloove (RNG) A2 O2
OW30* leptostachyus Boeckeler (Del Guacchio & Iavarone & Iavarone, 2012) Belgium, Limbourg (09.10.1983) 2148, Hoffman (RNG) G1 N10
OW31* leptostachyus (Del Guacchio & Iavarone, 2012) Belgium, Oost-Vlaanderen (16.09.1988) 5892, Goethebeur (RNG) G1 N1
OW32* leptostachyus (Del Guacchio & Iavarone, 2012) France, Cosne (01.09.1995) 17792, Dutartre (RNG) A1 N9
OW33* leptostachyus (Del Guacchio & Iavarone, 2012) France, Loiret (29.09.1979) 21798, Raynal (RNG) G1 N9
OW34† sativus Germany (2009) B1, (ÖBG) A1 O1
OW35† sativus Spain, Granada (2010) B4, Sibilio (NAP) A1 O1
OW36† sativus Spain, Valencia (2010) B3, Sepe (NAP) A1 O1
NEW WORLD
Central America NW1 hermannii (Buckley) Britton (Rebman, 2012) Mexico, Baja California (11.10.1980) 29313, Moran (SD – 106255) G1 N6
NW2 leptostachyus (Strong, 2000) British Virgin Islands, Anegada Island (29.10.1989) 45978, Proctor (US – 3399218) G1 N14
NW3 leptostachyus (Del Guacchio & Iavarone, 2012) Honduras, El Zamorano (05.06.1972) 27474, Molina (US – 2735228) A1 N3
NW4 leptostachyus (Schippers, 1994) Mexico, Zacatecas (14.08.1984) 36778, Wilbour (US – 3068201) G1 N3
NW5 leptostachyus (Schippers, 1994) Mexico, San Luis Potosi (18.08.1983) 7387, Kessler (US – 3103515) G1 N5
NW6 macrostachyus Boeckeler (Schippers, 1994) Bahamas, Nassau (20.04.1977) 48464, Correll (US – 2995910) A2 N5
NW7 macrostachyus (Strong, 2000) Puerto Rico, Isla de Vieques (11.11.1990) 46586, Proctor (US – 3209827) G1 N6
NW8 macrostachyus (Reznicek, 1985) Mexico, Cerro del Barreno (30.09.1967) 5342, Carter & Moran (US – 3313804) G1 N12
NW9 macrostachyus (Del Guacchio & Iavarone, 2012) Mexico, Molino de Rosas (04.08.1984) 4215, Ventura (US – 3194250) G1 N13
North America NW10 hermannii (Schippers, 1999) USA, Utah (09.1939) s.n., Parrish (US – 1825373) G1 N6
NW11 hermannii (Rebman, 2007) USA, California (12.09.2007) 13942, Rebman (CDA – 7861) G1 N5
NW12 hermannii (Rebman, 2005) USA, California (19.08.1935) s.n., Gander (SD – 12145) G1 N22
NW13 hermannii (Rebman, 2007) USA, California (12.09.2007) 13942, Rebman (SD – 182830) G1 N6
NW14 leptostachyus (Del Guacchio & Iavarone, 2012) USA, Mississippi (16.09.1991) 10977, Bryson (US – 3500573) G1 N15
NW15 leptostachyus (Del Guacchio & Iavarone, 2012) USA, California (10.08.1994) 1208, Strong & Kelloff (US – 3221968) G1 N8
NW16 leptostachyus (Del Guacchio & Iavarone, 2012) USA, Arizona (04.09.1948) 5165, Gould & Robinson (US – 2008779) G1 N1
NW17 leptostachyus (Schippers, 1994) USA, Colorado (18.08.1965) 1353, Richardson & Robertson (US – 3030224) G1 N2
NW18 leptostachyus (Reid, 2010) USA, Louisiana (22.06.2010) 7481A, Reid (LSU) G2 N4
NW19 leptostachyus (Strong, 1994) USA, Virginia (11.08.1992) 5651, Norn (US – 3284197) G2 N20
NW20 leptostachyus (Reid & Christopher, 2004) USA, Louisiana (24.09.2004) 5295, Reid & Christopher (LSU – 99742) G1 N2
NW21 leptostachyus (Ferguson et al., 2003) USA, Louisiana (20.09.2003) 1181, Ferguson et al. (LSU – 56815) G4 N17
NW22 macrostachyus (Reid, 2010) USA, Louisiana 5954, Reid (LSU) A1 N18
NW23 macrostachyus (Reid & Christopher, 2004) USA, Louisiana (06.08.2004) 5177, Reid & Christopher (LSU – 115827) G1 N6
NW24 macrostachyus (Reid et al., 2006) USA, Louisiana (06.09.2006) 5878, Reid et al. (LSU – 106199) G1 N7
NW25 macrostachyus (Schippers, 1994) USA, Florida (23.04.1973) 8349, Brumbach (US – 2751400) G1 N21
NW26 macrostachyus (Carter, 1999) USA, Oregon (13.07.1993) 4647, Halse (US – 3258359) G1 N6
NW27 macrostachyus (Godfrey, 1892) USA, Florida (24.10.1982) 84441, Godfrey (RBGE) G1 N4
South America NW28 leptostachyus (Pedersen, 1957) Argentina, Entre Rios (17.12.1957) 4747, Pedersen (US – 2283547) G1 N19
NW29 leptostachyus (Simon, 1998) Argentina, Entre Rios (21/22.12.1998) 47, Simon (US – 3505505) A1 N19
NW30 leptostachyus/esculentus (Del Guacchio & Iavarone, 2012) Ecuador, Puerto Jeli (16.02.1988) 70177, Laegaard (US – 3352883) G1 N11
NW31 leptostachyus (Schippers, 1994) Paraguay (05.1987) 4113, Schmeda (US – 3088045) G1 N19
NW32 leptostachyus (Gonto, 2002) Venezuela, Anzoategui (10.1996) 9656, Fernandez et al. (US – 3432848) A1 O2
NW33 leptostachyus (Schippers, 1994) Venezuela, Puerto Ayacucho (16.04.1978) 15128, Davidse & Huber (US – 3073713) A1 N20
NW34 macrostachyus (Pedersen, 1959) Paraguay (15.10.1959) 5127, Pedersen (US – 2432832) G1 O2
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*Introduced.

†Commercial product.

Fig. 1.

Fig. 1.

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The localities of the investigated Cyperus esculentus plants. Information is also shown for plastid DNA haplotypes (coloured symbols) and on the statistical parsimony network using TCS software. Each insertion/deletion (indel) was considered to be a single mutation event, and all indels were therefore coded as single positions in the final alignment. TCS was run with a default parsimony connection limit of 97 %. Black dots represent undetected haplotypes; the size of the shapes corresponds to the number of individuals that share the haplotype. Codes and legends corresponding to taxon names are as shown in Table 1.

Total genomic DNA was isolated from fresh leaves and tubers by using the procedures detailed in De Castro et al. (2012); a protocol by Andreasen et al. (2009) was used for DNA extractions from herbarium specimens by using approx. 50 mg of leaf tissue. The concentration was estimated by comparing 1 µL of DNA extract with a DNA standard (Marker II, AppliChem GmbH) on a 0·8 % agarose gel containing 0·5 µg mL–1 ethidium bromide (AppliChem GmbH) with the UVIdoc HD5 gel documentation system (UVITEC, Cambridge, UK).

PCR amplification and sequence analyses

Molecular markers were amplified by using primers that were reported in the literature and new primers designed for this study for nested-PCR (Table 2) (Macrogen Inc.). The volume of each reaction was 25 µL, with 5–10 ng of template for fresh tissue or 5 µL for herbarium tissue, 2·5 µL of 10× DreamTaq Buffer (Thermo Fisher Scientific Inc., Life Technologies), 0·5 µL each of the 2·5 mm nucleotides (Promega), 0·125 µL of 50 mm primer and 0·25 µL DNA DreamTaq polymerase (5 U µL–1) (Thermo Fisher Scientific Inc.). Amplifications of recalcitrant herbarium DNA templates were performed by using nested-PCRs with internal primers or HotStarTaq Plus DNA Polymerase (Qiagen). The cycling parameters of the PCRs were performed according to the manufacturer’s instructions in a GeneAmp PCR System 2700 thermal cycler (Applied Biosystems, Thermo Fisher Scientific Inc., Waltham, MA, USA) or in a MyCycler Thermal Cycler (Bio-Rad Laboratories, Hercules, CA, USA).

Table 2.

Primers used for PCR amplification and/or cycle sequencing of plastid and nuclear DNA regions of the Cyperus esculentus accessions sequenced in this study

Primer Sequence (5'–3') Reference
ndhF gene
Forward–F1 ATG GAA CAK ACA TAT SAA TAT GC Olmstead and Sweere (1994)
Reverse–F1318 CGA AAC ATA TAA AAT GCR GTT AAT CC Olmstead and Sweere (1994)
Forward–2F ACT CAT GCT TAT TCG AAA GC Graham et al. (1998)
Reverse–1.6R CCT ACT CCA TTG GTA ATT CCA T Graham et al. (1998)
rbcL gene
Forward-rbcL 1F ATG TCA CCA CAA ACA GAA AC Fay et al. (1998)
Reverse-rbcL 1460R TCC TTT TAG TAA AAG ATT GGG CCG AG Fay et al. (1998)
Forward-rbcL 636F GCG TTG GAG AGA TCG TTT CT Muasya et al. (1998)
Reverse-rbcL 674R GAT TTC GCC TGT TTC GGC TTG TGC TTT ATA AA Muasya et al. (1998)
rps16 intron
Forward-rpsF GTG GTA GAA AGC AAC GTG CGA CTT Oxelman et al. (1997)
Reverse-rpsR2 TCG GGA TCG AAC ATC AAT TGC AAC Oxelman et al. (1997)
Forward-CYPrps16F_int* CTA TAG TAA TGA AAA TGC TCT TGG This study
Reverse-CYPrps16R_int* ATT TTC ATC TCA TAC GGC TCA AG This study
ETS1f
Forward-ETS-F CTG TGG CGT CGT CGC ATG AGT TG Starr et al. (2003)
Reverse-18S-R AGA CAA GCA TAT GAC TAC TGG CAG G Starr et al. (2003)
Forward-cypETS-F_int* GGA CAT GCC TTG CAT GGC This study
Reverse-cyp18S-R_int* TCG YRT ATC RTT CGG GTC G This study
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*Nested-PCR.

Amplified products were purified by polyethylene glycol (PEG) 8000 precipitation (AppliChem GmbH), and approx. 10 ng per 100 bp of purified templates were sequenced according to the method of Di Maio and De Castro (2013) by using a fluorescent dye (Big Dye Terminator Cycle Sequencing Kit ver. 3.1, Applied Biosystems, Thermo Fisher Scientific Inc.) and a 3130 Genetic Analyzer (Applied Biosystems, Thermo Fisher Scientific Inc.). The sequences were analysed with AB DNA Sequencing Analysis ver. 5.2 software (Applied Biosystems, Thermo Fisher Scientific Inc.), edited in Sequence Navigator ver. 1.0.1 (ABI Prism, Perkin Elmer), assembled and aligned in BioEdit ver. 7.2.5 software (Hall, 1999). Alignments of rps16 haplotypes and ETS1f ribotypes are presented in Supplementary Data Files S1 and S2. The rps16 haplotypes and ETS1f ribotypes were identified according to variation in the aligned sequences (Tables 3 and 4). GenBank accessions for the sequences are reported in Tables 3 and 4.

Table 3.

Haplotypes detected in the rps16 alignment

Haplotype Base position
 GenBank accession no.
201 224 289 513–517 638
A1 G G C – A LK029864
A2 G G T – A LK029865
G1 G G C – G LK029866
G2 G T C – G LK029867
G3 A G C – G LK029868
G4 G G C TAAAA G LK029869
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The base position corresponds to alignments present in Supplementary Data File S1.

Table 4.

The ribotypes detected in the ETS1f alignment

Ribotype Base position
 GenBank accession no.
23 24* 34 62 120 130 139 142 163 185 202 203 251 263 282 293 307 317 346 353 354 357 379 381 386 391* 401
O1 G T C C T T T T G G T T A G A T G A C T C G A T G Y T LK029870
O2 G T C C T T T T G G T T A G A T G A C T C G A T G T T LK029871
O3 G T C C T T T T G G T T A G A T G A C T C G A T G C T LK029872
O4 G T C C T T T C G G T T A G A T G A C T C G A T G T T LK029873
O5 G T C C T T T T G G T T A G A T G A C T C G G C G T T LK029874
N1 C Y C C T C T T G A T T A G A T G A C T C G A T G Y T LK029875
N2 G Y C C T C T T G A T T A G A T A T C T C G A T G Y T LK029876
N3 G C C C T C T T G A C T A G A T G A C T C G A T G C T LK029877
N4 G Y C C T C T T G A T T A G A T G A C T C G A T G C T LK029878
N5 G C T C T C T T G A T T A G A T G A C G C G A T G C T LK029879
N6 G C T C T C T T G A T T A G A T G A C T C G A T G C T LK029880
N7 G C C C T C T T G A T T A G A T G A C T C G A T G C T LK029881
N8 G Y C C T T T T G G T T A G A T G A C T C G A T G C T LK029882
N9 G Y C C T C T T G A T T A G A T A A C T C G A T G Y T LK029883
N10 G Y C C T C T T G A C T A G A T G A C T C G A T G C T LK029884
N11 G T C C T Y T T G R T T A G A T G A C T C G A T G T T LK029885
N12 G Y C C T C T T G A G T A G A T G A C T C G A T G C C LK029886
N13 G C C C T C T T G A T T A G C T G A C T C G A T G C T LK029887
N14 G Y T C T C T T G A T T A G A T G T C T C G A T G Y T LK029888
N15 G Y C C T C T T G A T T A G C T G A C T C G A T G Y T LK029889
N16 T T C C T C T T G A T T A G T C G A T T T G A T A T T LK029890
N17 G T C A T C T T G A T T A G G T G T C T C G A T G C T LK029891
N18 G Y C C T C A T G A T T A T A T G A C T C G A T G C C LK029892
N19 T T C C T C T T G A T G A G A T A A C T C G A T G T T LK029893
N20 G T C C T T T T A G T T A G A T G A C T C G A T G T T LK029894
N21 G T C A A C T T G A T T A G A T G A C T C T A T G C T LK029895
N22 G C C C T C T T G A T T G G A T G A C T C G A T G C C LK029896
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The underlined nucleotides distinguish between the Old Word and New World accessions of Cyperus esculentus.

The nucleotides with asterisks are polymorphic in some accessions.

The base position corresponds to the alignment in Supplementary Data File S2.

For taxonomic details, see Table 1.

To check the monophyletic status of our ETS1f accessions, a phylogram was prepared with MrBayes ver. 3.1 software (Huelsenbeck and Ronquist, 2001; Ronquist and Huelsenbeck, 2003) and by using the ETS1f data set of Larridon et al. (2013). The Bayesian Markov chain Monte Carlo (MCMC) algorithm was run for 15 000 000 generations with two cold and four heated chains starting from random trees and sampling the trees every 2000 generations. The general time- reversible (GTR) model with a gamma-distributed rate (‘lset nst = 6, rates = gamma’) was used, according to the results obtained with jModelTest ver. 2.1.4 software (Darriba et al., 2012).

Statistical parsimony network

Genealogical relationships among the genotypes were inferred by using plastid rps16 haplotypes and nuclear ETS1f ribotype sequences, after sequencing other nuclear [internal transcribed spacer (ITS)] and plastid (trnL intron, trnF-trnL spacer, psbA-trnH spacer and the matK hypervariable region) markers failed to produce sufficient variation.

These relationships were examined by constructing a haplotype network using the parsimony method of Templeton et al. (1992) as implemented in TCS ver. 1.21 software (Clement et al., 2000). This method estimates the maximum number of substitutions to connect two haplotypes parsimoniously with a given confidence value. This approach is particularly useful for inferring relationships among genes with low divergence levels. The method also assigns an ‘outgroup probability’ based on the coalescent theory to each haplotype in the statistical parsimony network (Castello and Templeton, 1994). The likelihood of rooting is calculated as a function of the haplotype position in the network, its frequency and its number of connections with neighbour haplotypes (Castello and Templeton, 1994). Each insertion/deletion (indel) was considered to be a single mutation event, and all indels were therefore coded as single positions in the final alignment. TCS was run with a default parsimony connection limit of 97 %.

Biogeographical analysis

We used statistical dispersal–vicariance (S-DIVA) and Bayesian binary method (BBM) analyses implemented in RASP ver. 2.1b software to reconstruct the possible ancestral ranges of C. esculentus (Yu et al., 2013). We used the same Bayesian output data file employed in Larridon et al. (2013), which was kindly provided by Isabel Larridon. According to Larridon et al. (2013), 107 taxa (included C. esculentus) were used to detect phylogenetic relationships and generic delimitations in the C4 species of Cyperus (fig. 3 of Larridon et al., 2013). The chosen molecular markers were nrDNA (ETS1f) and plastid DNA (rpl32-trnL, trnH-psbA) sequences.

The distribution range of the data set of Larridon et al. (2013) was divided into nine areas, which were based on the presence of the species as reported in the World Checklist of Selected Plant Families (Kew database, http://apps.kew.org/wcsp/home.do) and the eFloras database (http://www.efloras.org/index.aspx). These areas are as follows: A (northern Europe), B (sub-tropical Europe), C (sub-tropical Asia), D (tropical Asia), E (sub-tropical/temperate Africa), F (tropical Africa), G (northern America), H (sub-tropical America) and I (tropical America).

The final consensus tree output obtained by Larridon et al. (2013) was used to run S-DIVA. The final tree was optimized with the ancestral range by using Scirpoides holoschoenus (L.) Soják as the outgroup.

Even if a restriction on the number of areas is inferred at internal nodes, it is recommended to reduce ambiguities at the more basal nodes of the tree (Ronquist, 1996, 1997). An analysis was performed to change the maximum number of possible areas at each node to seven (‘maxareas’ = 7), because the majority of the widespread species are common in seven areas {BCDEFHI; Cyperus compressus L., C. cuspidatus Kunth, C. laevigatus L., Kyllinga brevifolia Rottb. [=C. brevifolius (Rottb.) Hassk.], K. odorata Vahl [=C. sesquiflorus (Torr.) Mattf. & Kük.], Pycreus macranthus (Boeckeler) C.B.Clarke (=C. macranthus Boeckeler), P. polystachyos (Rottb.) P.Beauv. (=C. polystachyos Rott.) and Remirea maritima Aubl. [=C. pedunculatus (R.Br.) J.Kern]}.

The BBM analysis was also conducted in a similar way. MCMC analysis chains were run simultaneously for 15 000 000 generations. The state was sampled every 1000 generations. Fixed JC + G (Jukes-Cantor + Gamma) values were used for BBM analysis with outgroup root distribution.

Divergence time estimation

To determine the age of C. esculentus, a time-measured phylogenetic analysis in a Bayesian framework (Drummond et al., 2006) was performed by using the plastid DNA data set, which was kindly provided by Pascal-Antoine Christin and used for dating the evolution of C4 photosynthesis (Christin et al., 2008). The data set contained the original 320 species of Christin et al. (2008) plus the C. esculentus analysed here. Four C. esculentus taxa were analysed as representatives of its geographical range and haplotypic rps16 diversity [OW11, OW26, New World (NW) 18 and NW28] (Table 1). The GenBank accession numbers are listed in the Results. The resulting sequences were edited, assembled and aligned as indicated above. The analysis was performed by using BEAST ver. 1.7.5 software (Drummond et al., 2012). The GTR nucleotide substitution model was employed with a gamma-shaped parameter and a proportion of invariant sites (GRT + G + I) according to the guidelines indicated in Christin et al. (2008). Data from Besnard et al. (2009) were employed to calibrate the trees. Specifically, the ages for ‘C4 Cyperaceae’ (lineage no. 23) and for ‘C4 Fimbristylis’ (lineage no. 19) as indicated in table 1 of Besnard et al. (2009) were employed. A further calibration point, which was not directly indicated in the above-mentioned paper (the clade including ‘Sphaerocyperus’ and ‘Ascolepis c’ in fig. 1 of said paper) was obtained through the courtesy of P.-A. Christin. An uncorrelated lognormal relaxed clock model and a Yule prior model of speciation were assumed. The Bayesian MCMC procedure was run for 50 000 000 generations, with a burn-in of 5 000 000. Sampling was performed every 2000 generations. Tracer ver. 1.5 and TreeAnnotator ver. 1.7.5 software (Rambaut and Drummond, 2007) were used to analyse the posterior age distributions of the nodes of interest and to compute a maximum clade credibility tree.

RESULTS

Taxonomic treatment

Excluding the more distinct Cyperus esculentus var. sativus, the discrimination between intraspecific taxa by employing the keys provided by Schippers et al. (1995) was not always satisfactory. In fact, NW30 (Ecuador) has intermediate characters between C. esculentus var. esculentus and var. leptostachyus. In addition, some specimens were hard to refer to a single variety with sufficient accuracy, i.e. OW10 (var. esculentus, Zimbabwe), NW3 (var. leptostachyus, Honduras) and NW8–NW9 (var. macrostachyus, both from Mexico). However, the remaining portion of the sample can be identified at the varietal level by employing the above-mentioned taxonomic keys (Table 1). According to our analyses, the most useful characters in discriminating among the specimens were as follows: spikelet length, spikelet width, the maximum width of the floral scale in the middle of a spikelet, the distance from the base of the floral scale to the location of its maximum width, the medium length of the floral scale and the total length of the style. Generally, our identifications are congruent with the previous taxonomic determination.

Sequence analyses of rps16 and ETS1f

After editing, the alignment of rps16 intron sequences resulted in a matrix of 639 characters (633–639 bp) (Supplementary Data File S1) as follows: four single nucleotide polymorphisms (SNPs) and one indel were detected and six haplotypes were recognized (File S1 and Table 3), but no correlation with varieties or geography was detected (Table 1; Fig. 1). In fact, the most common haplotypes are G1 (58·57 % of total samples) and A1 (22·86 % of total samples), which are present in both the OW and NW Cyperus accessions (G1 = 44·4 %, A1 = 30·6 % of the OW sample and G1 = 73·6 %, A1 = 14·7 % of the NW sample); another haplotype present in both the NW and OW is A2 (5·71 % of the total sample), with 2·9 % in the NW and 8·3 % in the OW. Exclusive haplotypes for the NW are G2, which were detected only in northern America, and G4 (2·86 % and 1·43 % of total samples and 5·9 % and 2·4 % in NW samples, respectively). G3 is exclusive to the OW, with a frequency of 8·57 % of the total samples and 16·7 % for only the OW area.

The ETS1f nuclear DNA matrix had 427 characters (Supplementary Data File S2); 27 ribotypes (22 NW and 5 OW) were detected, due to 27 SNPs, two of which discriminated well between the NW and OW accessions (positions 130 and 185 bp, see File S2 and Table 4). These positions presented a thymine nucleotide (position 130 bp) and guanine nucleotide (position 185 bp) in all OW accessions, and a cytosine nucleotide (position 130 bp) and adenine nucleotide (position 185 bp) in NW accessions, with the exception of six specimens (NW15, NW19, NW30, NW32, NW33 and NW34), which can be ascribed to the OW nucleotide pattern. In addition, one accession (NW30) shows double peaks in these nucleotide positions, i.e. T/C (Y = 130 bp) and G/A (R = 185 bp). Other double peaks (Y) for a single nucleotide were detected in positions 24 bp and/or 391 bp for 14 NW and seven OW accessions (Tables 1 and 4). In the Bayesian inference phylogram obtained by using the ETS1f matrix of Larridon et al. (2013), all C. esculentus accessions form a monophyletic group with high posterior probabilities (PP = 1; Supplementary Data Fig. S3). As observed with plastid haplotypes, no genetic correlation between Cyperus varieties was detected, except for the distribution of the ribotypes, which is geographically structured in two groups as reported above.

Statistical parsimony network

Using TCS, a 97 % parsimony connection limit of eight steps was calculated for rps16 haplotypes, with six steps for ETS1f haplotypes and 10 steps for the combined data set. The plastid DNA network does not reveal a clear geographical structure (Fig. 1). No loops are present, and one haplotype, which was not found in the analysed individuals, is considered for hypothetical missing intermediates (black dot). Haplotype G1 has the highest outgroup probability (0·51) (Fig. 1).

Nuclear ETS1f data present a geographical variability partition between the OW and the NW (Fig. 2). Five positions in the network (NW lineages) are included in closed loops that could not be unambiguously resolved. These loops were each caused by single homoplastic alignment positions. Sixteen ribotypes, which were not found in the sample (1 = OW; 15 = NW) appear as hypothetical missing intermediates (black dots). The highest outgroup probability is associated with the OW ribotypes included in the rectangular box of the network (0·30) (Fig. 2). The combined network shows the same overall pattern as the nuclear DNA network, except that a larger number of genotypes is missing (26) and there are 14 loops (data not shown).

Fig. 2.

Fig. 2.

Open in a new tab

A parsimony network of nuclear ribotypes (ETS1f) is shown for Cyperus esculentus accessions using TCS software. Each insertion/deletion (indel) was considered to be a single mutation event, and all indels were therefore coded as single positions in the final alignment. TCS was run with a default parsimony connection limit of 97 %. Black dots depict missing intermediate ribotypes that were not found for the investigated individuals. Grey lines represent alternative ambiguous connections (loops). Codes and legends corresponding to taxon names are as shown in Table 1.

Biogeographical analysis

Both S-DIVA and BBM analyses suggest a biogeographical history in which dispersal has been crucial in shaping the current distribution pattern of C. esculentus (Supplementary Data Figs S4 and S5). S-DIVA suggests one possible ancestral range, with F (tropical Africa) for the node of C. esculentus (PP = 0·98), and the occurrence of this range is 100 % (Supplementary Data Fig. S4). BBM analysis postulates that the ancestor originated in tropical Africa (F) and/or sub-tropical Africa/tropical Africa (EF). The occurrence at its node was 38 % for F and 33 % for EF (plus 0·29 % of the undetermined area) (PP = 0·98) (Supplementary Data Fig. S5). Therefore, the dispersal of C. esculentus most probably started in tropical to sub-tropical African regions.

Divergence time estimation

The divergence time estimation of C. esculentus was computed by aligning rbcL and ndhF for our species to the data set of Christin et al. (2008). The rbcL and ndhF sequences of the four investigated C. esculentus accessions (see the Materials and Methods for details) exhibited a 100 % identity within our sample. The sequences of the newly sequenced genes from C. esculentus were deposited in GenBank under the following accession numbers: LK029901 (rbcL, OW11), LK029897 (ndhF, OW11), LK029902 (rbcL, OW26), LK029898 (ndhF, OW26), LK029903 (rbcL, NW18), LK029899 (ndhF, NW18), LK029904 (rbcL, NW28) and LK029900 (ndhF, NW28). By adding our C. esculentus sequences, the final data set included 321 sequences and 3774 characters (rbcL = 1401 bp; ndhF = 2373 bp).

The maximum clade credibility tree obtained from 50 000 000 MCMC generations (convergence was reached at approx. 5 000 000 generations) indicates that the most recent common ancestor between C. esculentus and its immediate outgroup has an age of 5.1 million years (Mya) [95 % highest posterior density (HPD) 2.5–10.2].

DISCUSSION

The literature offers an abundant range of hypotheses concerning the origin of Cyperus esculentus. Confusion is due especially to the fact that wild plant types have been discussed separately from the crop. According to several authors, the ancient edible variety may be of Mediterranean origin (e.g. De Vries, 1991; Negbi, 1992; De Felice, 2002), but all previous hypotheses on the origin of our plant of interest have been highly speculative. The difficulties in clarifying this issue, on which no general consensus among scholars is yet available, largely depend upon the ancient and widespread cultivation of this species, which may have obscured its biogeographical and evolutionary origin (Negbi, 1992; Pascual et al., 2000). However, botanical and historical evidence supports the hypothesis that the origin of the domesticated form occurred in a pool of wild plants that were native to the Mediterranean region (Negbi, 1992; Pascual et al., 2000; Defelice, 2002).

This sedge is a very pernicious weed, having become invasive in America, northern Europe, Asia and Australia (Auld and Medd, 1987; Konnai et al., 1990; ter Borg et al., 1998; Li et al., 2001; Milczak et al., 2001; Halvorson and Guertin, 2003; Holec et al., 2014). The success of C. esculentus as a weed may be attributed to several factors, including rapid clonal spread by tubers and rhizome extensions, which are difficult to eradicate (Anderson, 1999; Halvorson and Guertin, 2003), basal bulbs at the end of rhizomes, abundant flowers and seeds (Holm et al., 1977), seed/tuber longevity (Uva et al., 1997), seeds of variable viability (Hill et al., 1963; Thullen and Keeley, 1979; Stoller and Sweet, 1987), the fragmentation and flood dispersal of rhizomes (Anderson, 1999), C4 photosynthesis, allelopathic effects (Mulligan and Junkins, 1976; Anderson, 1999; Halvorson and Guertin, 2003; Heidarzade and Esmaeili, 2013) and phenotypic plasticity (Schippers et al., 1995), which makes the species difficult to control (and difficult to identify). In fact, according to Stoller and Sweet (1987), many biotype variations of this species are expected because they have probably adjusted to a multitude of local environments. Variations are observed in tuber dormancy and longevity, in rhizome and tuber development, in flowering and in herbicide responses.

Despite the variability of invasive types, notable eco-morphological differences are present between these and the cultivated forms, making the wild form a winner in natural selection (Dyer, 2006; Holec et al., 2014). However, if the varieties proposed by Schippers et al. (1995) allow for the identification of ‘wild’ C. esculentus from the NW and OW, then, as the authors themselves write, ‘the plasticity of C. esculentus can have consequences for determination of specimens. The effect of the environment can change the appearance of the plant drastically. Characters like spikelet length, width, ray length, bract length, and number of rays are all plastic. Since C. esculentus is a cosmopolitan species, this can easily lead to a wide range of morphological forms caused by interaction between environment and the different genotypes’. According to the morphological observations of the specimens employed here, the OW accessions are morphologically less variable and can be distinguished more easily (excluding those of presumable recent introduction from the NW) in comparison with NW accessions; in the latter, in fact, various intermediate characters are observed. The reduced variation of OW forms has also been confirmed with our molecular analyses.

Our molecular results show considerable variation in the substitution rates between the employed nuclear and plastid markers, as already documented by Larridon et al. (2011, 2013). The different patterns observed between plastid and nuclear markers reveal that the two types of markers convey different levels of information. The low mutation rate in plastid DNA is coherent with the current haplotype distribution in which no geographical structure is displayed, but which includes information on the dispersal pattern (see below). In nuclear DNA, if we exclude the varieties that were recently introduced back to the OW (Guillerm, 1987; De Vries, 1991; ter Borg and Schippers, 1992), two ribotypes are detected, with an evident geographical segregation, namely an OW group and a polymorphic NW group (Fig. 2). As a consequence of the weak resolution of our data at this level of detail, we refrain from making detailed comments on the relationships among the single NW and OW individuals.

The high genetic variability in the American ribotypes does not exhibit any correlation with taxonomic varieties (C. esculentus vars leptostachyus, macrostachyus and heermannii); however, the variability found in the NW may certainly be related to the enormous plasticity of this plant, which is also able to colonize a great diversity of environments (sub-tropical to cold areas). Our data on the genetic diversity of C. esculentus in the NW are in line with reports on random amplified polymorphic DNAs (RAPDs) by Okoli et al. (1997) and on isoenzymes by Horak and Holt (1986) and Holt (1994); all these authors documented extensive variability at the molecular level and suggested that it reflects variation in phenological and morphological traits. The same analyses were also performed on OW populations, but with discordant results [RAPD, Abad et al., 1998; amplified fragment length polymorphism (AFLP), Dodet et al., 2008].

American varieties also kept their variability when recently introduced in Europe (Guillerm, 1987; De Vries, 1991; ter Borg and Schippers, 1992). In fact, we maintain that these introductions changed the genetic make up of C. esculentus, resulting in an uncontrolled invasion in cold areas and subsequently in the rest of Europe, with the formation of new genotypes, most probably introgressed with OW forms, which are more competitive relative to the native forms (C. esculentus vars esculentus and sativus) (Schippers et al., 1993; ter Borg et al., 1998; Li et al., 2001; Milczak et al., 2001). According to ter Borg et al. (1998), an important ecological difference exists between NW and OW specimens of C. esculentus, from which the OW C. esculentus is incapable of spreading from its primary area to establish itself in more northern and colder countries, unlike the American varieties.

To understand the phylogeographic patterns for C. esculentus over its whole range, it is essential to locate the origin of the species and to define the direction of intercontinental dispersal events in a precise geological time scale. As shown in the Results, the divergence time estimation for the origin of C. esculentus ranged from the end of the Miocene to the beginning of the Pliocene (5·1 Mya; 95 % HPD = 2·5–10·2). Given this time range, the most likely evolution of C4 photosynthesis in the Cyperus lineage (stem-group = 10·9 Mya; Besnard et al., 2009) and major plate tectonic events are at best distantly involved in the distribution of our species, whereas long-distance dispersal (LDD) adaptations, reproductive strategies of C. esculentus, the patterns of Atlantic ocean currents over the last million years and the development of agriculture probably played a major role. The resulting time frame also excludes major vicariance events [e.g. the Gondwanan break up of 160–30 Mya (Upchurch, 2008; Christenhusz and Chase, 2013)].

Our biogeographical inferences suggest that the ancestral range of the ancestor of what we today recognize as C. esculentus must have originated in the OW, with great probability in Africa [tropical = 100 % (S-DIVA), 38 % (BBM); sub-tropical–tropical = 33 % (BBM)], and that subsequent dispersal led to the present distribution of this plant. A plausible scenario would be the following: African plants on the stem lineage of C. esculentus reached America by LDD followed by diversification. Timing this/these events is beyond the scope of this paper, but a Columbian exchange is most probably excluded (at least for the earliest events) because, according to the literature, this plant was used by native Americans as a source of food during the early Holocene (Hart and Ives, 2013) and by the Maya during the pre-Columbian period (Fedick, 2010). In addition, we suggest that the large number of ribotypes detected in the NW would be in agreement with the idea that dispersal to the NW was not recent; on the contrary, we can explain the plastid pattern (which was uncorrelated to continental distribution; see Fig. 1) as a consequence of multiple independent colonization events over time. Multiple LDD events have also been documented for other amphi-Atlantic sedges (Roalson and Friar, 2004; Escudero et al., 2008). In the light of multiple dispersal events, we avoid making speculations about the presence of some OW ribotypes in the NW (Figs 1 and 2). Given the nature of our sampling, which was not aimed at a fine-scale investigation, it would be difficult to understand whether those ribotypes are direct descendants of the OW founder ribotypes or of a more recent introduction.

With respect to LDD, three general major mechanisms of dispersal between Eurasia and America have been suggested, i.e. the North Atlantic Land Bridge, the Bering Land Bridge and the Atlantic route (Ridley, 1930; Raven and Axelrod, 1974; Janis et al. 2004; Renner, 2004; de Queiroz, 2005). The migration of C. esculentus to America via the North Atlantic Land Bridge is highly unlikely, because this land bridge dates back to the early Oligocene (Tiffney, 1985; Xiang et al., 2005), and even the last connections through Iceland and the Faroe Islands disappeared during the early mid Miocene (15 Mya; Milne and Abbot, 2002). As suggested for other species of sub-tropical origin (e.g. Cennamo et al., 2013), the climate would also have constituted a major obstacle, given the major cooling episode (the mid Miocene disruption) that occurred during that period (Miller and Fairbanks, 1983). We are not inclined to consider dispersion via the Bering Land Bridge as probable either. Cyperus esculentus was historically absent from northern Asia; at least its OW forms are intolerant of cold climates, and the Bering Land Bridge occurred during the glacial maxima. The Atlantic route seems more probable, because it has no specific temporal or climatic constraints, even though no special LDD syndrome has been described for C. esculentus. However, unspecialized diaspores and small seeds can also be subject to LDD (Allessio et al., 2005; Tackenberg et al., 2006; Escudero et al., 2009; Vargas et al., 2014). Concerning the modality of LDD, a review by Renner (2004) on the times and mode of plant dispersal across the tropical Atlantic emphasized that trans-Atlantic dispersal by water (in both directions) appears to be more common than dispersal by wind or birds. Cyperus esculentus may well have been dispersed by water, because its rhizomes, stolons and even achenes and seeds can float (Anderson, 1999; Halvorson and Guertin, 2003). Mats made of tangled plant material, including fruits, rhizomes and seeds, are constantly carried out into the tropical Atlantic from the deltas of the Congo, Senegal and Amazon rivers, and some enter the conveyor belt-like currents transporting debris in either direction across the Atlantic (Renner, 2004). For example, the minute seeds of Miconia argentea (Melastomataceae) crossed the Atlantic in soil stuck to drifting vegetation (Dalling et al., 1998). However, the small diaspores (achenes and seeds) of C. esculentus can also be dispersed by wind and birds (Anderson, 1999; Halvorson and Guertin, 2003). In Juncus bufonius (Juncaceae), a species that is similar in terms of diaspore size, Ridley (1930) showed that the seeds are carried in mud by adhering to the feet of birds. In addition, sedge achenes tend to remain viable in the faeces of birds after retention in the digestive system (e.g. 37 h in C. ochraceus; DeVlaming and Proctor, 1968).

When C. esculentus reached the NW, it had already been subjected to different selective pressures that most probably contributed to shaping its genetic diversity. In fact, its settlement in new geographical regions may expose a species to novel ecological conditions that facilitate the establishment and diffusion of new genotypes and morphotypes (e.g. via hybridization and/or polyploidization) as indicated by various sources (Levin, 1983; Heiser and Whitaker, 1948; Rath and Patnaik, 1978; Arias et al., 2011). This finding may explain the appearance of cold-adapted C. esculentus, which colonized a large number of habitats in northern America and became one of the most pernicious weeds in the world (Bryson and Carter, 2008). Later, reproductive isolation may have facilitated morphological and genetic divergence between the NW and OW forms.

In conclusion, our molecular analysis provides novel insights into the evolutionary history of C. esculentus. The data reported here have various taxonomic and phylogenetic implications, including the absence of molecular support for taxonomic varieties and a hypothesis on the origin and phylogeography of this species, which probably originated during the late Cenozoic in Africa, and repeatedly reached the Americas, largely independent of Columbian exchanges. Future work on a wider sample, including natural populations more than single herbarium specimens from the whole range of the species, carried out using different molecular techniques (e.g. nuclear microsatellites and/or SNPs), will probably allow an increased resolution, especially in the relationships among the NW plants and among individuals/populations of different ploidy. Population-wide collection will also allow a modern morphometric assessment of the morphological diversity of this polymorphic species to be carried out and to be compared with molecular variation.

SUPPLEMENTARY DATA

Supplementary data are available online at www.aob.oxfordjournals.org and consist of the following. File S1: alignments of rps16 haplotype sequences. File S2: alignments of ETS1f ribotype sequences. Figure S3: a Bayesian inference phylogram obtained by using the ETS1f sequences of our Cyperus esculentus specimens and the data set from Larridon et al. (2013) (PP above 60 % are shown). The accepted species names according to Larridon and Goetghebeur (2013), Bauters et al. (2014), Govaerts et al. (2014), Larridon et al. (2014) are reported in parentheses. Figure S4: a majority-rule consensus tree from the Bayesian inference analyses (Larridon et al., 2013) and dispersal– vicariance scenarios for Cyperus esculentus as reconstructed by statistical dispersal–vicariance (S-DIVA) optimization. Vicariance event (star) and dispersal event (rhomb). The accepted species names according to Larridon and Goetghebeur (2013), Bauters et al. (2014), Govaerts et al. (2014), Larridon et al. (2014) are reported in parentheses. Figure S5: the majority-rule consensus tree from Bayesian inference analyses (Larridon et al., 2013) and dispersal–vicariance scenarios for Cyperus esculentus as reconstructed by Bayesian binary method (BBM) analysis. Vicariance event (star); dispersal event (rhomb); and extinction event (triangle). The accepted species names according to Larridon and Goetghebeur (2013), Bauters et al. (2014), Govaerts et al. (2014), Larridon et al. (2014) are reported in parentheses.

Supplementary Data
supp_115_5_733__index.html (892B, html)

ACKNOWLEDGEMENTS

We gratefully acknowledge Dr Siny J. ter Borg for providing the references that were quite difficult to find and for his most helpful suggestions at an early stage of this work; and Dr Pascal-Antoine Christin (Department of Animal and Plant Sciences, University of Sheffield, UK) and Dr Isabel Larridon (Department of Biology, Ghent University, Belgium), who provided their complete data files. The authors are also grateful to Dr Valentina Iavarone, Dr Filomena Sepe and Luca Paino for technical assistance in the laboratory and to Dr Roberta Vallariello, curator of the Herbarium Neapolitanum (NAP) (Department of Biology, University of Naples Federico II, Italy).

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