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Phylogeographic patterns and possible incipient domestication of Jacaratia mexicana A. DC. (Caricaceae) in Mexico

Genetic Resources and Crop Evolution, 2010
Juan Ramirez
Pablo Cuevas
Oscar Dorado
Esau Leyva
Lupis Altamirano
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Phylogeographic patterns and possible incipient domestication of Jacaratia mexicana A. DC. (Caricaceae) in Mexico

Phylogeographic patterns and possible incipient domestication of Jacaratia mexicana A. DC. (Caricaceae) in Mexico

    Juan Ramirez
    Pablo Cuevas
    Oscar Dorado
    Esau Leyva
    Lupis Altamirano
Genet Resour Crop Evol (2010) 57:1227–1238 DOI 10.1007/s10722-010-9569-1 RESEARCH ARTICLE Phylogeographic patterns and possible incipient domestication of Jacaratia mexicana A. DC. (Caricaceae) in Mexico D. Arias • J. Pen˜aloza-Ramı´rez • O. Dorado • P. Cuevas-Reyes • Esau´ Leyva • Ana Luisa Albarra´n-Lara • G. Rangel-Altamirano Received: 2 November 2009 / Accepted: 6 May 2010 / Published online: 9 June 2010 Ó Springer Science+Business Media B.V. 2010 Abstract Jacaratia mexicana A. DC. (Caricaceae) and cultivated populations utilizing chloroplast DNA is a tropical tree distributed throughout Mexico and and nuclear DNA sequences. We generate a Bayesian Mesoamerica. Some evidence in Mexico indicates the phylogenetic tree, to estimate the divergence time presence of an incipient domestication process in this between clades using calibrated mutation rates. We species. Phylogeographical analyses can potentially also infer the demographic history of these popula- determine contemporary patterns of gene flow, iso- tions using neutrality tests among wild and cultivated lation between population lineages, as well as accessions. We identified higher levels of haplotype historical processes such as population bottlenecks and nucleotide diversity for the cpDNA and ITS types or expansions on their geographical areas. In this in wild populations than in domesticated populations. study we reconstruct the phylogeographical patterns These results indicate a reduction of genetic diversity in populations of J. mexicana A. DC., in order to find derived from human selection on domestication differences between genetic variation among wild traits. Neutrality test suggests population expansion detected by the significant negative values of Fu’s Fs in the cultivated populations of this specie. These process results in an excess of rare polymorphism with the fixation of certain advantageous mutation throughout time, this implication are in accordance D. Arias  O. Dorado  E. Leyva  G. Rangel-Altamirano Centro de Educacio´n Ambiental e Investigacio´n Sierra de with the role of the strong selection in the fruit traits Huautla, Universidad Auto´noma del Estado de Morelos, of J. mexicana. The dated phylogeny constructed Avenida Universidad 1001, Colonia Chamilpa, with BEAST program indicated a dispersion pattern 62210 Cuernavaca, Morelos, Me´xico for the J. mexicana ancestors across the South Pacific J. Pen˜aloza-Ramı´rez (&)  A. L. Albarra´n-Lara and South Eastern populations during the late Plio- Laboratorio de Ecologı´a gene´tica, Centro de cene. Posterior dispersion and divergence in the Investigaciones en Ecosistemas, Universidad Nacional clades from Central Mexico and North Pacific are in Auto´noma de Me´xico UNAM, Antigua Carretera a agreement with the episodes of mountain-building in Pa´tzcuaro No. 8701, Colonia San Jose de la Huerta, 58190 Morelia, Michoaca´n, Me´xico different regions of Mexico. e-mail: jpenaloza@oikos.unam.mx Keywords cpDNA  ITS types  Domestication  P. Cuevas-Reyes DNA sequences  Tajima’s D  Fu’s FS, Bayesian Facultad de Biologı´a, Universidad Michoacana de San Nicola´s de Hidalgo, Francisco. J. Mu´gica, Colonia relaxed clock method BEAST, Mexico  Felı´citas del Rı´o, C.P. 58030 Morelia, Michoaca´n, Me´xico Jacaratia mexicana 123 1228 Genet Resour Crop Evol (2010) 57:1227–1238 Introduction variation (Dane and Lang 2004; Hillman and Davies 1990; Miller and Schaal 2006). This process occurs Insights about genetic variation within species are an during a domestication bottleneck (reduction of essential factor to explain the distribution of biolog- genetic diversity) as result of artificial selection in ical diversity (Caicedo and Schaal 2004; Schaal et al. domesticated species (Dane and Lang 2004). For 1998). The distribution of this variation is frequently example, several domesticated plant crops showed a regulated by factors such as ecological events, reduction in the amount of genetic diversity in selective processes or by the patterns of contempo- domesticated populations, given that have been rary genetic exchange (Avise 2000). Phylogeographic exposed to a recent and strong selection event, at approach provides powerful analysis to clarify pro- numerous loci during domestication processes (Gepts cesses such as the genealogical relationship between and Papa 2002; Hamrick and Godt 1997). Crops such haplotypes as well as their geographical distribution as maize show several cases of selection because (Avise 2000), furthermore, can potentially determine there are often several genes involved in single processes such as population bottlenecks or expan- morphological traits (Wright and Gaut 2005). Nev- sions (Schaal et al. 1998). Nevertheless, a small ertheless, little is known about the effect of artificial amount of phylogeographic studies have investigated selection in domesticated species in terms of popu- the genealogical relationship and the divergence time lation connectivity and demography in areas with between populations or species (Brown et al. 2008; higher species richness. Mexico is considered one of Crandall et al. 2008; Guo and Ge 2005; Jakob et al. the Vavilov’s centers of domestication species in the 2009; Moore and Donoghue 2007; Stock et al. 2008), world (Harlan 1975; Heiser 1979; Vavilov 1926), it in some way due to the unavailability of physical has been estimated that before the Spanish coloniza- historical data such as fossil records in many lineages tion, the pre-Hispanic settlements in Mesoamerica of plants or animals (Brown et al. 2008). Recently, were utilized more than 105 plant species of several methods have been performed to evaluate economic importance (Miranda and Herna´ndez-X molecular sequence differences such as the develop- 1963; Rzedowski and Equihua 1987). Some examples ment of relaxed molecular clock methods (Rutsch- of plants species that have their origin or domestica- mann 2006). These methods require assumptions tion in Mexico are: maize (Benz 2001), beans about the demographic processes and a substitution (Koenig and Gepts 1989), chilies (Walsh and Hoot mutation rate of sequence evolution (Drummond 2001) among others. Nevertheless, in Mexico despite et al. 2006). Several studies have used this method- of high diversity less attention have been focused ology to determine divergence time in Nerita (Crand- about how the domestication processes have modu- all et al. 2008), Bufo (Stock et al. 2008), in lated the extent and distribution of the genetic Adoxaceae and Valerianaceae (Moore and Donoghue variation in wild and domesticated populations 2007) and in domesticated crops such as rice Oryza (Sanders and Price 1968; Heiser 1979). (Guo and Ge 2005). Jacaratia mexicana A. DC. (Caricaceae), ¨Bonete,¨ Domesticated plants are expected to be good is a tropical unisexual tree (dioecious) that measures models to evaluate the demographic and historical up to 14 meters in height and is distributed from processes that potentially might occur through Mexico to Nicaragua and El Salvador (Moreno domestication. Domestication events include human 1980). In Mexico, the distribution ranges from sea selection of individuals with the best characteristics level to 1500 meters, from the Pacific slope from of interest such as sweeter fruits, bigger tubers, longer Nayarit, Jalisco, Michoacan; the basin of Rio Balsas fibers, etc. (Doebley 1989; Gepts and Papa 2002). in Guerrero, Morelos, and Oaxaca; to the central The consequence of this artificial selection is that depression of Chiapas and the Yucatan Peninsula cultivated populations represent a sub-sample of the (Standley 1924). Some evidence has been found in genetic pool variation present in wild conditions J. mexicana which suggest that this specie is under- (Doebley 1989; Hamrick and Godt 1997). For going an incipient domestication syndrome (i.e. instance, trees cultivated in orchards exhibit less morphological and physiological changes in culti- genetic variability than trees cultivated in backyard vated individuals in contrast to their wild ancestors). gardens, which display intermediate levels of genetic The majority of trees of Bonete are found in wild 123 Genet Resour Crop Evol (2010) 57:1227–1238 1229 conditions, but in several localities on the states of sampled in Northern Pacific and Central Mexico Nayarit, Jalisco, Michoaca´n, Guerrero and Morelos, (Table 1). In order to identify the phylogenetic tree are commonly found in backyard gardens and family root, we include two possible outgroups that in orchards (Rzedowski and Equihua 1987). In these previous studies, such as Aradhya et al. (1999) have regions the Bonete fruit is highly valued as a been considered as closely related species: Jacaratia complementary foodstuff. The seeds are sold in dolichaula (Donn. Sm.) Woodson and Carica papaya traditional markets as food (Niembro 1986). The L. From each individual five mature leaves were grated stem mixed with maize, was used for the sampled and then stored at -80°C in the laboratory manufacture of tortillas (Moreno 1980; Standley for molecular analysis. Genomic DNA was extracted 1924), the Olmecas and Tlahuicas used the leaves from 100 mg of leaf material using the protocol to tenderize meat (Briones 2002). The diversity of designed by the Dneasy Plant method QIAGEN. All common names suggests that this species has been DNA samples were amplified using PCR technique, utilized by several cultures in Mexico (Guizar and for the chloroplast intergenic spacers we selected the Sa´nchez 1991; Rzedowski and Equihua 1987), but at regions atpB-rbcL and trnL-trnF, while for the present time they are cultivated and sold only on local nuclear genome; we used Internal Transcribed Spacer scales. (ITS). The amplifications and DNA sequencing were In this study, (1) we infer population structure on the developed using the primers atpB-F and rbcL-R basis of a haplotype network; (2) estimate divergence (Chiang et al. 1998). The trnL-trnF primers used were times between inferred clades using calibrated muta- trnL and trnF (Ferna´ndez et al. 2001). For the ITS we tion rates; (3) infer the demographic history of these utilized the primers ITS1 and ITS4 the rDNA spacers, populations using neutrality tests, and (4) compare separating 18S, 5.8S and 26S rDNA genes (Baldwin diversity and demographic history among wild and 1992; White et al. 1990). Polymerase chain reactions cultivated accessions. The main questions are: What were carried out in a volume of 25 ll containing are the geographical or historical features that may 20 ng of template DNA, 2 mM MgCl2, 10 mM Tris– explain the observed population structure (or the lack HCl (pH 9), 0.1 mM of each dNTP, 0.5 mg ml 21 thereof) and demographic history? Are the patterns of bovine serum albumin, 2 mM of each primer and genetic variation among wild and cultivated accessions 0.3 ll of TaqDNA polymerase (Gibco, Invitrogen, consistent with a process of incipient domestication in San Diego, CA, USA). The thermal cycling condi- Jacaratia mexicana? tions consisted of one cycle denaturation at 95°C for 2 min, 30 cycles of 1 min at 95°C, 1 min annealing at 50°C, and 1.5 min extensions at 72°C. PCR Materials and methods products were purified using the method QIAquickTM from QIAGEN. Finally, the samples were run in an Plant sampling, DNA extraction, PCR automatic sequencer ABI PRISMÒ 310 Genetic amplification and sequencing Analyser. Nucleotide sequences were edited and aligned with the program SequencherÒ v. 4.9 for In total we collected 200 individuals of J. mexicana the three DNA regions. In total we obtained in 176 A. DC. in 25 localities (Fig. 1) that represented four individuals 1140 bp for the concatenating atpB-rbcL geographic regions: (1) North Pacific coast ‘‘NP’’ that and trnL-F spacers, and in 200 individuals 678 bp for includes populations from Nayarit, Jalisco and Coli- the ITS spacers. ma; (2) Central Mexico ‘‘CM’’ that included local- ities from Michoaca´n, Guerrero, State of Mexico, and Diversity analysis Morelos; (3) Southeastern ‘‘SE’’ that content popu- lations from Veracruz, Campeche and the Yucatan In order to compare the levels of inter and intrapop- Peninsula, and finally (4) Southern Pacific coast ‘‘SP’’ ulation genetic diversity, we estimate the number of which contains populations in Chiapas, and Oaxaca. haplotypes (h), haplotype diversity index (Hd), Individuals were sampled from wild habitats in the nucleotide diversity per site (p) and the number of Southeastern and South Pacific Coast regions, and polymorphic segregating sites (S) between wild and domesticated habitats such as family orchards were cultivated populations of J. mexicana utilizing the 123 1230 Genet Resour Crop Evol (2010) 57:1227–1238 Fig. 1 Geographic distribution from Jacaratia mexicana A. DC. populations. Note: location of the four geographical regions in dashed colors, which correspond to those populations listed in the Table 1 DNASP 5.1 program (Rozas and Rozas 1999). We populations of J. mexicana, using the Bayesian performed neutrality test in order to investigate about relaxed clock method in BEAST 1.5.3 program possible historical demographic fluctuations such as (Drummond et al. 2006). BEAST analysis was population growth in populations of J. mexicana. performed for both DNA regions, for the concate- Particularly we performed a neutrality test Fu’s FS nated alignment of AtpB-rbcL/trnL-F (1140 pb) and which detected an excess of recent substitution events for ITS (678 pb) data set. We utilize a relaxed produced by population growth (Fu 1996), all these lognormal model of lineage rate variation; and a test were developed with ARLEQUIN 3.11 program model of nucleotide substitution GTR (General time (Excoffier et al. 2005) with 104 permutations. Pair- reversible, Tavare´ 1986) which was obtained from wise population genetic differentiation FST was Akaike information criteria (AICc) performed with estimated among defined geographic regions and Modeltest 3.7 program (Posada and Crandall 1998). between wild and cultivated populations, this analysis Nevertheless, no fossil records are currently available was performed in ARLEQUIN 3.11 program (Excof- for time calibrations in the family Caricaceae. In fier et al. 2005) with 104 permutations. consequence, we selected two calibrations based on absolute mutation rates available: for non-coding Haplotype network and divergence times cpDNA regions a mutation rate of 7 9 10-9 substi- tutions per year (Richardson et al. 2001; Wolfe et al. We construct both haplotype networks for each DNA 1987) was chosen, and the mutation rate for the region (e.g. cpDNA AtpB-rbcL/trnL-F and for nu- nuclear ITS was utilized at 8 9 10-9 substitutions clearDNA the ITS) using Median-Joining Network, per year (Richardson et al. 2001; Wolfe et al. 1987). this method combines the topology of a minimum In all BEAST analysis, we performed four replicate spanning tree with a MP (Maximum Parsimony) analyses of 156 generations to ensure the convergence search to identify and remove unnecessary links of the MCMC chain. We evaluated the sampling among haplotypes, all these methods were performed distributions of each run in TRACER 1.5 program in NETWORK 4.5 program (Bandelt et al. 1995). (Drummond et al. 2006) and then combine the log Additionally, we estimated the divergence time in files from each run to ensure the stable posterior 123 Genet Resour Crop Evol (2010) 57:1227–1238 1231 Table 1 Summary statistics and neutrality test for Jacaratia (Hd), Nucleotide Diversity (p) and the number of polymorphic mexicana populations. Regional cpDNA and ITS frequencies, segregating sites (S). Neutrality test Fu’s FS measure departure population number, populations status (Cultivated and Wild), from neutrality sample sizes (n), number of haplotypes (h), haplotype diversity Region Populations cpDNA haplotypes ITS type s Cultivated n H Hd p S FS n h Hd p S FS North Nayarit (1,2) 16 2 0.400 0.0011 3 -19.3* 16 2 0.400 0.0006 1 -27.9* Pacific Jalisco (3) 8 8 Colima (4) 8 8 Cultivated Central Michoacan 24 4 0.580 0.0015 6 -26.2* 32 3 0.471 0.0011 2 -34.0* Mexico (5,6,7,8) Guerrero (9,10,11) 24 24 E. Mexico (12,13) 8 16 Morelos (14) 8 8 Wild South Veracruz (15) 8 6 0.869 0.0101 30 -13.1 8 2 0.507 0.007 1 -3.0 Eastern Campeche (16,17) 16 16 Yucatan 24 32 (18,19,20,21) Wild South Chiapas (22) 8 4 0.800 0.0063 15 -7.68* 8 1 0.200 0.002 0 -29.0 Pacific Oaxaca (23,24,25) 24 24 Total 176 16 0.911 0.0088 47 2.351 200 4 0.611 0.0014 3 1.081* * Statistical significant distribution in all parameter estimates using Log- individuals in an alignment length of 678 bp nuclear Combiner 1.5. Furthermore, we construct a consensus sequences. 666 bp were constants and only 3 parsi- of trees with a maximum credibility and node height mony informative sites (Table 1), the haplotype distributions which was constructed in TreeAnnotator diversity Hd was 0.61, the polymorphic segregating 1.5, and then was visualized and edited in FigTree 1.3 sites was 3 and nucleotide diversity p was 0.0014. The program (Rambaut 2006). comparison between the wild and cultivated subsam- ples (for both DNA regions) revealed that the haplo- type diversity (Hd), nucleotide diversity (p) and the Results number of polymorphic segregating sites (S) are significantly higher in wild populations (e.g. South Genetic diversity Eastern cpHd = 0.86, nHd = 0.50, cpp = 0.01, np = 0.007, and cpS = 30, nS = 1, and South Pacific In 25 populations of Jacaratia mexicana through cpHd = 0.80, nHd = 0.20, cpp = 0.006, np = 0.002, Mexico we detected 16 haplotypes for the concate- and cpS = 15, nS = 0) than in cultivated ones (e.g. nated alignments of atpB-rbcL and trnL-F in the Central Mexico cpHd = 0.58, nHd = 0.47, cpp = cpDNA regions, which results in 1140 bp in 176 0.0015, np = 0.001, and cpS = 6, nS = 2, and North individuals. 1064 were constant, and 47 were parsi- Pacific cpHd = 0.40, nHd = 0.40, cpp = 0.0011, mony informative sites (Table 1). The haplotype np = 0.0006, and cpS = 3, nS = 1), indicating a diversity Hd was 0.91, the polymorphic segregating reduction in the amount of genetic diversity (Table 1). sites S was 47 and the nucleotide diversity p was 0.008. The values of genetic differentiation between For the nuclear DNA, we found four ITS types in 200 geographic regions are moderately differentiated 123 1232 Genet Resour Crop Evol (2010) 57:1227–1238 Table 2 Pairwise population differentiation FST between divergence time between predefined geographical groups, above the lines genetic differentiation for the nuclear regions of J. mexicana (Figs. 2a and 3a) were ITS, below the lines pairwise FST for the cpDNA performed utilizing the absolute rate for non-coding North Central South South cpDNA regions at 7 9 10-9 substitution per position Pacific Mexico Eastern Pacific per year and 8 9 10-9 for nuclear DNA regions North – 0.4871 0.1391 0.7818 (Richardson et al. 2001; Wolfe et al. 1987). Infer- Pacific ences for the species outgroup J. dolichaula and Central 0.4617 – 0.1160 0.6385 C. papaya showed a mean age estimated for the Mexico divergence time of 3.5 My (95% credibility interval South 0.4658 0.4176 – 0.5583 ‘‘CI’’); North Pacific and Central Mexico clades Eastern shown estimates between 1.3 and 2.0 My (95% CI); South 0.5455 0.5324 0.3190 – Central Mexico and South Eastern clades resulted in Pacific a divergence time ranging between 2.0 and 3.9 Mya, (95% CI); Central Mexico and South Pacific shown (Table 2) among wild and cultivated populations estimates around 2.0–4.3 My (95% CI); finally, the (NP/CM cpFST = 0.46, nucFST = 0.48; NP/SE divergence between South Eastern and South Pacific cpFST = 0.46, nucFST = 0.13; NP/SP cpFST = 0.54, shown a divergence time ranged from 3.9 to 4.3 My nucFST = 0.78; CM/SE cpFST = 0.41, nucFST = (95% CI). All estimates ranging between late Plio- 0.11; versus CM/SP cpFST = 0.53, nucFST = 0.63). cene, Pleistocene and the Holocene epoch (Figs. 2 and 3). Population demographic inferences Neutrality test analysis (Fu’s Fs) provides insights Discussion about the evolutionary demographic history (Table 1). For both DNA regions, the AtpB-rbcL/trnL-F and ITS Genetic diversity were suggested population growth in North Pacific and Central Mexico geographic regions, because Fu’s Fs In this study, we identified cpDNA and nuclear ITS test are negative and significant which signifies an genetic variation in the populations of Jacaratia excess in the number of rare alleles, indicating a mexicana (Table 1). From the parameters of diversity population expansion. The neutrality test of South such as the haplotype diversity and nucleotide Eastern and South Pacific populations for both genes diversity, we observed high levels of genetic diversity (Table 1) showed negative values but not significant in wild populations from South Eastern cpHd = 0.86, for the test Fu’s Fs. nHd = 0.50, cpp = 0.01, np = 0.007, and South Pacific cpHd = 0.80, nHd = 0.20, cpp = 0.006, Haplotype network and divergence times np = 0.002, than in domesticated populations from Central Mexico cpHd = 0.58, nHd = 0.47, cpp = The haplotype networks from nuclear DNA (four 0.0015, np = 0.001, and North Pacific cpHd = 0.40, haplotypes) and chloroplast DNA (16 haplotypes) nHd = 0.40, cpp = 0.0011, np = 0.0006. This infor- data, showed similar patterns in the distribution of mation suggests the role that plays artificial selection haplotypes in the populations (Figs. 2b and 3b). We during domestication process, thus results in a included in both networks the same outgroups (i.e. progressive reduction of genetic diversity in culti- J. dolichaula and C. papaya) utilized in BEAST vated ones (Dane and Lang 2004; Doebley 1989; analysis. We observe that populations from South Hamrick and Godt 1997), given that have been Pacific and Southeastern Mexico are the most ancient exposed to a recent and strong selection event, at lineages, with other derived haplotypes to Central numerous loci during domestication (Gepts and Papa Mexico and South Pacific. Also, we found ancestral 2002; Innan and Stephan 2000). The differences in haplotypes widely spread in several geographic the amount of genetic diversity provide evidence regions, where numerous recent haplotypes are about wild habitats, as potential reservoirs of genetic derived. On the other hand, the estimations for the variation (Caicedo and Schaal 2004; Hillman and 123 Genet Resour Crop Evol (2010) 57:1227–1238 1233 Fig. 2 a Comparative timing of divergences for J. mexicana C. papaya, and hatched bars represent populations of South based on relaxed clock methods BEAST (cpDNA). The scale Eastern, South Pacific, Central Mexico and North Pacific bar is divided up by time (in millions of years before present) respectively as were described in the Fig. 1. b Median-Joining according to the Late Pliocene, Pleistocene, and Holocene network constructed in Network 4.5 epoch. The black squares are outgroups J. dolichaula and Davies 1990; Koenig and Gepts 1989). In J. mexi- process involve in most cases a limited amount of cana slight genetic diversity differences were found seed that reduce the genetic diversity of this species between cultivated and wild populations, but also, the (Dane and Lang 2004; Ellstrand et al. 1999; Gepts genetic differentiation shows more genetic structure and Papa 2002), whereas the natural dispersion of in wild populations FST than domesticated popula- J. mexicana promotes more genetic diversity in wild tions FST (Hamrick and Godt 1997; Miller and Schaal populations. 2006). The management practice plays an important role in the maintenance of genetic differentiation, in Population demographic inferences contrast with the natural dispersion in wild habitats (Hamrick and Godt 1997; Miller and Schaal, 2006). Neutrality test in wild populations from South Eastern For instance, in wild populations the natural disper- and South Pacific geographic regions indicates Fu’s Fs sion of J. mexicana has been mediated mainly by the negative estimates but not significant values (Table 1) white-nosed coati Nasua narica L. which have and are considered as evidence of populations having operated as effective seed dispersal (Valenzuela and evolved under neutrality, and without significantly Ceballos 2000). In contrast, in domesticated popula- increasing in size (Ramos-Onsins and Rozas 2002; tions of this specie, we found some evidences that the Wright and Gaut 2005). In contrast, tests of neutrality human transported the fruits across different Mexican Fu’s FS in domesticated populations from North localities (Briones 2002; Rzedowski and Equihua Pacific and Central Mexico geographic regions 1987). The patterns of dispersion in the domestication (Table 1) resulted in negative Fu’s Fs values as an 123 1234 Genet Resour Crop Evol (2010) 57:1227–1238 Fig. 3 a Comparative timing of divergences for J. mexicana C. papaya, and hatched bars represent populations of South based on relaxed clock methods BEAST (nDNA). The scale Eastern, South Pacific, Central Mexico and North Pacific bar is divided up by time (in millions of years before present) respectively as were described in the Fig. 1. b Median-Joining according to the Late Pliocene, Pleistocene, and Holocene network constructed in Network 4.5 epoch. The black squares are outgroups J. dolichaula and indicator of population expansion (Innan and Stephan genetic diversity, via domestication bottleneck e.g. 2000). These process results from the association of reduction in genetic diversity derived from human one common haplotype with others in lower frequen- selection on domestication traits (Doebley 1989; cies or with private haplotypes (Harpending et al. Hamrick and Godt 1997). Hillman and Davies 1993), and are frequently attributed to populations that (1990) showed that different factors, such as the have undergone recent range expansion (Rogers and fluctuation in the effective population size, the amount Harpending 1992). The frequency and distribution of of genetic diversity, and the strength of artificial changes resulted in an excess of rare polymorphism selection can modulate the evolutionary pathways and with the fixation of certain advantageous mutation time of domestication process. throughout time (Ramos-Onsins and Rozas 2002). These results are in agreement with the role of the Divergence time strong selection in the fruit traits of J. mexicana such as sweet and big fruits with considerable more flesh In the phylogenetic-dated tree constructed for both surrounding the seed observed in the North Pacific and DNA regions with BEAST program, the outgroups Central Mexico populations (Guizar and Sa´nchez included in this study Jacaratia dolichaula and 1991; Standley 1924). These processes, reduced Carica papaya (Figs. 2 and 3) indicate the most 123 Genet Resour Crop Evol (2010) 57:1227–1238 1235 oldest divergence time for this lineage ranged about without significant increasing in size (Harpending 3.5 My. In a previous phylogenetic study Aradhya et al. 1993). The further dispersion of Southern et al. (1999) found a strong phylogenetic relationship populations across Central Mexico and North Pacific between the genus Carica and Jacaratia. They may have occurred fairly later, as suggests the hypothesized as well, that the probable dispersion divergence time of this clade (1.75 My). These of a papaya ancestor from South America and Central dispersions were favored by the suitable climatic and America toward North American continent occurred geological events during the late Pliocene and with the relatively recent formation of the Isthmus of Pleistocene (Metcalfe et al. 2000), such as the Panama 3 My ago (Aradhya et al. 1999; Raven and formation of the Sierra Madre Occidental Mountains Axelrod 1974). In accordance with this hypothesis, (Rossotti et al. 2002), the uplift of the Mexican we suggest a south-north colonization patterns of plateau (Graham 1999) and the development of the Jacaratia mexicana ancestors about 3.0 My, in the tropical or semiarid, dispersal corridor that linking late Pliocene. This scenario was supported by the Central Mexico and Northern Pacific geographic basal position of the Southern Mexico lineages (e.g. regions as were suggested by the pollen records in South Pacific and South Eastern) in the dated these geographic regions (Lozano-Garcia and phylogeny but also for the haplotype network Xelhuantzi-Lopez 1997, Rossotti et al. 2002). The (Figs. 2b and 3b) and showed a divergence time dispersal scenarios in the Holocene epoch suggested about 3 My. At this time, the pollen records for the presence of suitable habitat for the arrival of Central Mexico and South Pacific basins suggest tropical dry forest elements such as Mimosa and warm-humid climate conditions as deduced by the Bursera (e.g. Chalco Lake, Central Mexico) which presence of some mesophytic taxa (Lozano-Garcı´a share ecologically similar conditions to J. mexicana and Ortega-Guerrero 1997) and tropical dry forest (Lozano-Garcia and Xelhuantzi-Lopez 1997; Met- plant species (Piperno et al. 2007). These dry calfe et al. 2000). About 2000 years ago the first environmental conditions were possibly promoted human settlements were established in different by two main factors, the progressive reduction of regions of Mexico (Sanders and Price 1968) encour- humidity and volcanic activity in the area (Lozano- aging the development of domestication process in Garcı´a and Ortega-Guerrero 1997). These conditions several domesticated plants (Lo´pez and Luja´n 2001) possibly encourage the dispersion from Southern such as maize (Benz 2001), pumpkins (Smith 1997) populations of J. mexicana throughout South Eastern, beans (Koenig and Gepts 1989) chilies (Walsh and Central Mexico and North Pacific geographic Hoot 2001) among others. In J. mexicana there is regions. The posterior divergences between South some indication, that about 1200 years ago Olmecas Eastern and South Pacific lineages probably occurs and Tlahuicas from the state of Guerrero (Central about 1.75 My ago (Figs. 2 and 3) in the beginning of Mexico) used the leaves to tenderize meat brought Pleistocene. At this point in time, when a historical back from the hunt (Briones 2002). Our own climatic barrier in the Southern populations of evidence suggests that J. mexicana is undergoing an J. mexicana, such as the presence of temperate-forest incipient domestication processes. We observe higher across the Northeast mountains in the Sierra Madre levels of genetic diversity in wild conditions, than in del Sur (Graham 1999; Metcalfe et al. 2000) as were trees commonly found in backyard gardens and suggested by the pollen records that indicate pre- family orchards. Neutrality test Fu’s FS analysis in dominantly cold climate with more winter precipita- domesticated populations from North Pacific and tion than present (Van Devender 1990). These Central Mexico geographic regions (Table 1) resulted environmental conditions which probably exerted a in negative values as an indicator of population vicariant effect in the pattern of distribution between growth (Innan and Stephan 2000). These process both regions disrupting the gene flow among these results from the association of one common haplo- populations. Also interesting the moderate genetic type with others in lower frequencies or with private differentiation observed among these regions. Signals haplotypes (Harpending et al. 1993), and are fre- of fluctuation in the populations were non-significant quently associated to populations that have under- for the test Fu’s FS that also are considered as gone a recent population expansion (Rogers and evidence that populations evolved under neutrality, Harpending 1992). The frequency and distribution of 123 1236 Genet Resour Crop Evol (2010) 57:1227–1238 these changes resulted in an excess of rare polymor- Avise JC (2000) Phylogeography. The history and formation of phism with the fixation of certain advantageous species. Harvard University Press, Cambridge Baldwin BG (1992) Phylogenetic utility of the internal tran- mutation throughout time (Ramos-Onsins and Rozas scribed spacers of nuclear ribosomal DNA in plants: an 2002). Our own evidence suggests that in J. mexicana example from the Compositae. Mol Phylogenet Evol 1: the fruits have been target of human selection during 3–16 the domestication process. 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