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Genetic Variation and Evolution of Polaskia Chichipe

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Genetic Variation and Evolution of Polaskia Chichipe Molecular Ecology (2005) 14, 1603–1611 doi: 10.1111/j.1365-294X.2005.02494.x GeneticBlackwell Publishing, Ltd. variation and evolution of Polaskia chichipe (Cactaceae) under domestication in the Tehuacán Valley, central Mexico ADRIANA OTERO-ARNAIZ,*‡ ALEJANDRO CASAS,* JAMES L. HAMRICK† and JENNIFER CRUSE-SANDERS†§ *Centro de Investigaciones en Ecosistemas, Universidad Nacional Autónoma de México, Campus Morelia. Apdo. Postal 27-3 (Xangari) Morelia 58089, Michoacán, México, †Departments of Plant Biology and Genetics, 2502 Plant Sciences, University of Georgia, Athens, Georgia 30602, USA Abstract Polaskia chichipe is a columnar cactus under artificial selection in central Mexico because of its edible fruits. Our study explored the effect of human manipulation on levels and distribution of genetic variation in wild, silviculturally managed and cultivated sympatric populations. Total genetic variation, estimated in nine populations with five microsatellite ± loci, was HT = 0.658 0.026 SE, which was mainly distributed within populations (HS = 0.646) with low differentiation among them (FST = 0.015). Fixation index (FIS) in all populations was positive, indicating a deficit of heterozygous individuals with respect to Hardy– Weinberg expectations. When populations were pooled by management type, the highest ± expected heterozygosity (HE = 0.631 0.031 SE) and the lowest fixation index (FIS = 0.07) ± were observed in wild populations, followed by cultivated populations (HE = 0.56 0.03 SE, FIS = 0.14), whereas the lowest variation was found in silviculturally managed populations ± (HE = 0.51 0.05 SE, FIS = 0.17). Low differentiation among populations under different management types (FST 0.005, P < 0.04) was observed. A pattern of migration among neigh- bouring populations, suggested from isolation by distance (r2 = 0.314, P < 0.01), may have contributed to homogenizing populations and counteracting the effects of artificial selection. P. chichipe, used and managed for at least 700 generations, shows morphological differen- tiation, changes in breeding system and seed germination patterns associated with human management, with only slight genetic differences detected by neutral markers. Keywords: columnar cacti, crop evolution, dinucleotide repeats, domestication, genetic resources, genetic structure, microsatellites Received 4 May 2004; revision received 3 September 2004; accepted 12 January 2005 cacti (Casas et al. 1999, 2002). Currently, people in the Introduction region gather fruit from 20 species of columnar cacti from The semiarid Tehuacán-Cuicatlán Valley, central Mexico wild populations. They also practice silvicultural manage- has been identified as a key location for the origins of ment of wild populations of 12 species in situ that involves agriculture and plant domestication in the New World favouring individuals with useful phenotypes when natural (MacNeish 1967). People of this region domesticated a vegetation is cleared for agriculture (Casas et al. 1999). number of plant species including species of columnar Seven of these species are also cultivated in home gardens and terraces, mainly through vegetative propagation (Casas et al. 1999, 2001). Correspondence: Adriana Otero-Arnaiz, ‡Present address: Depart- Both cultivation and silvicultural management may ment of Biological Sciences, Indiana University, South Bend IN 46634-7111, USA; Fax: 574-520-6589; E-mail: [email protected]. involve domestication processes (Casas et al. 1999) that can §Present address: Rancho Santa Ana Botanic Garden, 1500 N. lead to phenotypic divergence between wild and mani- College Ave., Claremont, CA 91711, USA. pulated populations (De Candolle 1882; Darwin 1883; Zohary © 2005 Blackwell Publishing Ltd 1604 A. OTERO-ARNAIZ ET AL. 1984; Harlan 1992). Plant domestication and human another month between silvicultural and cultivated popu- manipulation of populations occur at varying intensities lations resulting in partial temporal isolation among these and can result in a continuum of morphological, physio- populations (Otero-Arnaiz et al. 2003). logical, and genetic differentiation between wild and In other species of columnar cacti studied, genetic struc- partially or fully domesticated variants. Studies of both ture among populations, measured as GST, was usually incipient and advanced degrees of domestication contrib- low. The only exception being Lophocoreus schotti, which ute to an understanding of how the process of evolution has a relatively high GST among populations from separate under artificial selection operates. They also allow for eval- geographical regions in Sonora and Baja California, Mexico uation of the impact of the current traditional management (Hamrick et al. 2002). Given the known patterns of man- on genetic diversity. Columnar cacti in the Tehuacán agement, artificial selection, and reproductive biology of Valley are ideal biological systems for studying ongoing P. chichipe, as well as the patterns of genetic structure domestication processes and genetic interactions through reported for other columnar cacti, we explored the follow- gene flow among wild and domesticated populations. ing topics: (i) the effects of management practices on genetic Fruits of these plant species are the primary targets of diversity of this cactus species; (ii) the effect of migration artificial selection, and farmers select on phenotypic in relation to geographical distance in the genetic structure characters such as fruit size, pulp colour and flavor, peel of populations; (iii) the levels of inbreeding among popu- thickness, and thorniness (Casas & Barbera 2002). lations under different management types. According to Polaskia chichipe (Glosselin) Backeberg is one of the previous studies on reproductive biology in P. chichipe columnar cacti species under silvicultural management (Otero-Arnaiz et al. 2003), the level of inbreeding was pre- and cultivation in the Tehuacán Valley (Casas et al. 1999). dicted to be higher in manipulated populations than in Recent studies (Carmona & Casas 2005) documented that wild populations. artificial selection has led to morphological differentiation This study used microsatellites to survey the genetic vari- among populations under different forms of management. ation and structure of wild, silvicultural and cultivated On average, fruits from cultivated populations are signi- populations of P. chichipe. The results are interpreted in the ficantly larger with more pulp, and contain larger and more light of information derived from studies of morphological numerous seeds than those from silviculturally managed variation (Carmona & Casas 2005) and reproductive bio- populations. On the other hand, fruits and seeds from logy (Otero-Arnaiz et al. 2003) to improve understanding silviculturally managed populations are larger than those of the evolutionary consequences of human management from unmanaged wild populations (Carmona & Casas of P. chichipe populations. 2005). Furthermore, artificial selection favoured individuals that were able to produce seeds through self-pollination Materials and methods leading to higher selfing rates among managed plants than nonmanaged individuals. This pattern was evident in Populations, individuals and plant tissue sampled pollination experiments. A longer fruit production season, as well as faster and higher percentage of seedling germi- A total of nine populations (three wild, three silviculturally nation, was also found in populations manipulated by managed, and three cultivated) were sampled within and humans (Otero-Arnaiz et al. 2003). around the villages of San Luis Atolotitlán, Caltepec, and Populations under silvicultural management and cul- Metzontla, in the state of Puebla, Mexico (Fig. 1). Flower tivation are derived from wild populations and all coexist buds were collected from 30 individuals per population in the same geographical area. Artificial selection on and maintained at −70 °C until DNA extraction. A method silviculturally managed populations of P. chichipe involves recommended for DNA extraction of cactus (De la Cruz tolerating, enhancing in abundance or propagating desir- et al. 1997), modified for miniprep, was used. able individuals while clearing nondesirable individuals from agricultural fields and pastures. Propagation of Microsatellite development and genotyping desirable individuals is conducted by sowing seeds and sometimes by planting branch cuttings (Carmona & Casas Five microsatellite loci were identified specifically for 2005). Polaskia chichipe. Three of them were described previously Genetic differentiation among P. chichipe populations (Otero-Arnaiz et al. 2004), and two were developed de novo was expected because previous experiments with crosses following the same procedure (Table 1). Polymerase chain among and within populations demonstrated that fruit reactions (PCRs) were performed using 7.5-µL reactions: production was more successful when pollen was donated 50–100 ng of DNA, 0.25 mm each dNTP, 2.5 mm MgCl2, from the same population (Otero-Arnaiz et al. 2003). 0.5 µm of each primer (fluorescent with either FAM, HEX Additionally, flowering peaks occur with a difference of or TET), 0.25 unit of Taq DNA polymerase (Perkin-Elmer), 1 month between wild and silvicultural populations and and 1 × Taq buffer (Perkin-Elmer), 1 × Taq master buffer. © 2005 Blackwell Publishing Ltd, Molecular Ecology, 14, 1603–1611 GENETIC CLUES IN DOMESTICATION OF P. CHICHIPE 1605 Mating patterns To estimate levels of selfed vs. outcrossed offspring among maternal
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