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(A–I) Images of the nine Opuntia species analyzed on this work. (C,E) Species O. huajuapensis and O. pilifera putative parentals of O. tehuacana, as proposed by Arias et al. (2012). Photos by X. Granados and S. Arias.
Source publication
The process of hybridization occurs in approximately 40% of vascular plants, and this exchange of genetic material between non-conspecific individuals occurs unequally among plant lineages, being more frequent in certain groups such as Opuntia (Cactaceae). This genus is known for multiple taxonomic controversies due to widespread polyploidy and pro...
Citations
... Several authors consider that species of the Opuntia genus hybridize easily because individuals with intermediate morphologies are present in cultivated fields (Bravo-Hollis, 1978; Gallegos-Vázquez and Mondragón, 2011) and some wild populations (Griffith, 2001;Granados-Aguilar et al., 2021). However, intermediate morphological characters may be insufficient to determine hybridization events (Rieseberg and Carney, 1998), because microclimatic conditions can lead to morphological variation in wild populations (Cordell et al., 1998;Angert et al., 2010;López-Borja et al., 2017). ...
... Opuntia streptacantha, a widespread species from the series Streptacanthae, is positioned as a sister group of some Basilares members (Martínez-González et al., 2022). Interclade reticulation has been reported (Majure et al., 2012;Granados-Aguilar et al., 2021), indicating the possibility of hybridization events among the studied species. We expect that prepollination events (flowering, stigma receptivity and pollen release) will not prevent interspecific pollen flow among the four species. ...
Premise
Barriers at different reproductive stages contribute to reproductive isolation. Self-incompatibility (SI) systems that prevent self-pollination could also act to control interspecific pollination and contribute to reproductive isolation, preventing hybridization. Here we evaluated whether SI contributes to reproductive isolation among four co-occurring Opuntia species that flower at similar times and may hybridize with each other.
Methods
We assessed whether Opuntia cantabrigiensis, O. robusta, O. streptacantha, and O. tomentosa, were self-compatible and formed hybrid seeds in five manipulation treatments to achieve self-pollination, intraspecific cross-pollination, open pollination (control), interspecific crosses or apomixis, then recorded flowering phenology and synchrony.
Results
All species flowered in the spring with a degree of synchrony, so that two pairs of species were predisposed to interspecific pollination (O. cantabrigiensis with O. robusta, O. streptacantha with O. tomentosa). All species had distinct reproductive systems: Opuntia cantabrigiensis is self-incompatible and did not produce hybrid seeds as an interspecific pollen recipient; O. robusta is a dioecious species, which formed a low proportion of hybrid seeds; O. streptacantha and O. tomentosa are self-compatible and produced hybrid seeds.
Conclusions
Opuntia cantabrigiensis had a strong pollen–pistil barrier, likely due to its self-incompatibility. Opuntia robusta, the dioecious species, is an obligate outcrosser and probably partially lost its ability to prevent interspecific pollen germination. Given that the self-compatible species can set hybrid seeds, we conclude that pollen–pistil interaction and high flowering synchrony represent weak barriers; whether reproductive isolation occurs later in their life cycle (e.g., germination or seedling survival) needs to be determined.
... In order for successful interspecific or extensive intergeneric crossing within a specific genus to occur (Eeckhaut et al., 2006) [31} , a number of hurdles must be overcome. More and more studies are highlighting the importance of these data as an important indicator to predict crossing efficiency in breeding programs as has been shown for example in Geranium (Akbarzadeh et al., 2021) [32] , Helleborus (Meiners and Winkelmann, 2012) [33] and Hydrangea (Granados-Mendoza et al., 2021) [34] . After postzygotic fertilization, numerous interspecific crosses exhibit issues such lower growth vigor, embryo abortion, endosperm development defects, or albinisms. ...
Plant breeding for crops and ornamentals has grown in importance over the past century. Mendel's theories about the inheritance of characteristics established the groundwork for contemporary genetics. While chromosomal duplication, mutation breeding, and intra-and interspecific cross-breeding remain the mainstays of ornamental plant breeding, plant breeding has advanced dramatically since Mendel's day. Advanced accuracy breeding and selection towards more challenging to measure or quantify characteristics are now possible because to new genomic techniques. The breeding of ornamental plants nowadays is a challenging endeavor with constantly evolving and new obstacles. Collaborations between research and industry will be necessary to apply current technology to small-scale crops.
... Tacinga has many taxonomic controversies due to natural hybridization or introgression between several of its species; thus, delimitation has been difficult. Population genetics of sympatric species and proposed hybrids would help understand reticulate evolution and species delimitation in Tacinga; at least, Granados-Aguilar et al. (2021) demonstrated that it is useful in some species of a closely related genus. ...
A new species of Tacinga from semi-arid Eastern Brazil, Tacinga paiaia, is here described on the basis of material collected several years ago and cultivated at the Cactarium Guimarães Duque of the Instituto Nacional do Semi-árido. A detailed description, original illustrations, distribution map, a taxonomic discussion for the new taxon, and a key to all known species of Tacinga are given. We also assessed
the IUCN risk of extinction category for the new species. It is here preliminarily classified as Vulnerable to extinction due to its small population size and restricted distribution. Finally, we also report the presence of extrafloral nectaries in the pericarpel areoles of the new taxon.
... While naturally occurring intergeneric hybrids are uncommon within the Cactaceae, interspecific hybridization is recurrent within many genera. Majure et al. (2012, Granados-Aguilar et al. (2021), and Majure (2022) uncovered rampant hybridization in Opuntia and suggested that many of the polyploids in that genus are likely derived from interspecific hybridization, although homoploid hybridization, i.e. hybridization without genome duplication, is much more poorly documented (Majure and Puente 2014 Baker andPinkava 1987, 1999;Fenstermacher 2016, Mayer et al. 2000, Pinkava 2002, reviewed in Machado 2008. ...
The rare Baja California Sur endemic cactus Grusonia robertsii was originally hypothesized to be an intergeneric hybrid between G. invicta and Cylindropuntia alcahes subsp. alcahes but was described as a Grusonia due to its overall closer resemblance to G. invicta, except in the fruit. A more comprehensive analysis of the morphology and phylogenetic placement of G. robertsii based on plastid and nrDNA sequences has revealed that Rebman's original hypothesis was correct, and this taxon represents the first documented intergeneric hybrid between Cylindropuntia and Grusonia, with G. invicta as the maternal parent and C. alcahes subsp. alcahes as the paternal contributor. We here describe a new nothogenus, Cylindronia, and provide a new combination for the nothospecies Cylindronia robertsii comb. nov.
... and also cited bees as pollinators (hummingbirds as the main pollinator; Lambert et al., 2006) and bees or hummingbirds for species Opuntia Desv. (Granados- Aguilar et al., 2020) from the desert and dry forests in Brazil and Mexico. In Costaceae, the two studied species of Costus L. from rainforest in Central America (Kay, 2006;Surget-Groba et al., 2013) were associated with pollination by long-billed hermit hummingbirds (Phaethornis longirostris). ...
Coevolution between floral traits and specific pollination behaviour is a significant evolutionary force in angiosperm diversification. However, hybridization is also reported to occur between plants with specialist pollination syndromes. Understanding the role of pollinators in plant diversification is crucial, especially in megadiverse regions, such as the Neotropics. In this review, we examine plant hybridization studies in the Neotropics with the aim of providing a perspective on biotic and abiotic factors starting hybrid zone formation. The Pleistocene was the most widely cited time for the occurrence of hybridization facilitated by geographical range shifts, but time-calibrated analyses are needed to recover a more realistic scenario. Our synthesis of hybridization and pollination systems suggested that specialist and generalist pollinators were associated with the starting point of hybridization in the Neotropical flora. Bees and hummingbirds are most likely to be the primary vectors of interspecific gene flow, and even sporadic visits by bees or other generalist pollinators could allow the formation of a new hybrid zone. We highlight that seed and pollen dispersal vectors should be included in an integrative discussion on hybridization in the Neotropical flora. We also provide a preliminary map of hybrid zones in the Neotropics, including Brazilian vegetation cover and losses in the last 30 years, with the aim of encouraging research into human-driven anthropogenic changes and formation and/or shift of hybrid zones through time.
... (Hunt et al. 2006;Arias et al. 2012). An important finding is that some O. tehuacana individuals have introgression from O. decumbens and O. huajuapensis, discarding O. pilifera as a putative parental species (Granados-Aguilar et al. 2021). Furthermore, O. tehuacana has variable characteristics throughout its distribution, such as the color of the flowers, the shape of the stem segments, the presence of hairs, and the length and number of spines, and because of this, certain populations were described as new species but later considered synonyms (Arias et al. 2012). ...
... Furthermore, O. tehuacana has variable characteristics throughout its distribution, such as the color of the flowers, the shape of the stem segments, the presence of hairs, and the length and number of spines, and because of this, certain populations were described as new species but later considered synonyms (Arias et al. 2012). Opuntia tehuacana inhabits the same area as O. decumbens, O. depressa Rose, O. huajuapensis, O. lasiacantha, O. pilifera, and O. velutina F.A.C. Weber (Arias et al. 2012;Granados-Aguilar et al. 2021), and similar to many wild opuntias from this biosphere reserve, its phylogenetic relations and ploidy remain unknown. In this study, we aimed to infer the phylogenetic position of O. tehuacana in the context of its sympatric species and to analyze genome evolution by estimating ploidy levels and genome sizes in five O. tehuacana populations. ...
... To avoid excess mucilage, we followed the modifications reported by Bustamante et al. (2016). We amplified one individual from seven Opuntia species ( Fig. 1; Supplementary Table 1) and 12 individuals from O. tehuacana for the plastid genes matK and ycf1 and the intergenic spacer psbJ-petA using the primers reported by Majure et al. (2012c), with some modifications in the amplification protocol of ycf1 and psbJ-petA, and for the nuclear introns AT3G48380 and AT1G18270 as reported by Granados-Aguilar et al. (2021). All PCRs were performed in 15 µL with the Platinum Taq commercial mix (Invitrogen). ...
Abstract
This study is focused on the Tehuacán-Cuicatlán Valley (Oaxaca, Mexico), which has a high diversity of Opuntia species
whose phylogenetic relationships and chromosome numbers are mostly unknown. We aimed to investigate the phylogenetic
position of Opuntia tehuacana and its sympatric species and to analyze the ploidy levels in fve O. tehuacana localities.
We performed phylogenetic analysis under Bayesian inference using three chloroplast markers (matK, ycf1 and psbJ-petA)
and two nuclear introns (AT3G48380 and AT1G18270) as well as chromosome counts for three Opuntia species and fow
cytometry analysis in O. tehuacana. In a broad phylogenetic context, O. tehuacana is a member of the Basilares clade, as
are most of its sympatric species, except for Opuntia decumbens, Opuntia lasiacantha, and Opuntia huajuapensis, which
are in the Nopalea clade. The comparison between nuclear and plastid trees showed incongruences for the positions of the
eight analyzed Opuntia species, although the O. tehuacana clade was recovered by both analyses. Furthermore, the phylogeny of nuclear evidence showed a geographic structure congruent with the sampled localities for O. tehuacana. The ploidy
levels of O. tehuacana are 11x and 12x, the highest reported thus far for the genus, whereas for Opuntia pilifera it is 8x and
for O. huajuapensis it is 2x. Finally, we found that the signifcant diferences among O. tehuacana genome sizes and the
high ploidy level might be due to multiple polyploidization events occurring between individuals from the same species
and involving other Opuntia species.
Keywords Aneuploidy · Hybridization · Interspecifc gene fow · Polyploidy · Tehuacán-Cuicatlán Valley
... Some examples include phylogenetic analyses carried out in the tribes Cacteae (Vázquez-Sánchez et al. 2013) and Hylocereeae (Korotkova et al. 2017), as well as the genera Astrophytum (Vázquez-Lobo et al. 2015), Cephalocereus (Tapia et al. 2017), Opuntia (Majure et al. 2012b) and Pereskia (Butterworth & Wallace 2005). Phylogenetic relationships for the above mentioned tribes and genera are better understood, but there are still other groups in this family in which relationships at the genus or species level have not been resolved due to processes such as incomplete lineage sorting (ILS) or hybridization (Majure et al. 2012b, Copetti et al. 2017, Granados-Aguilar et al. 2021. ...
Background: Hybridization in nature occurs in numerous botanical families. In particular, the Cactaceae family contains lots of genera in which hybridization is reported.
Questions: What are the patterns of reported natural hybridization in Cactaceae and their probable causes? Are there phylogenetic and evolutionary implications related to hybridization, particularly in Opuntioideae?
Data description: A total of 62 articles about natural hybridization and classical Cactaceae literature were reviewed.
Study site and dates: From 1900 to June 2021
Methods: A search for articles was performed in Web of Science and Google Scholar with the keywords "Cactaceae hybridization", for time span "1900 to 2021" and included information from classic family-specific monographs.
Results: Natural hybrids in Cactaceae occur in subfamilies, Cactoideae and Opuntioideae. There is evidence of nonselective mechanisms of reproductive isolation, but only for few taxa. For Cactoideae members the main approach used was morphological description, and the tribe with the highest number of natural hybrids was Trichocereeae. In Opuntioideae, the reviewed articles performed mostly chromosome counts, morphometric and phylogenetic analyses, and showed the highest number of natural hybrids.
Conclusions: It has been suggested that hybridization impacts the evolution of Cactoideae and Opuntioideae, but few studies have formally tested this hypothesis. In Cactoideae, we found only descriptive evidences of hybridization; therefore, previous statements suggesting an important role of hybridization in the evolution of Cactoideae should be supported by performing formal analyses. For the postulation that hybridization impacts the evolution of Opuntioideae, we found formal evidence supporting hybridization hypothesis unlike what we found in Cactoideae.
... Qualitative character states used in the multivariate analysis of Pilosocereus leucocephalus group s.s For the AT1G18270 intron, we used the c primers(Granados-Aguilar et al. 2021) with a temperature profile of 94 °C for 2 min; 36 cycles of 94 °C for 32 s, 56.5 °C for 30 s, and 72 °C for 1 min and 10 s; and a final extension of 72 °C for 5 min. Finally, the PCR cleaning and Sanger sequencing was performed at the Laboratorio de Biología Molecular de la Biodiversidad y de la Salud, Instituto de Biología, UNAM. ...
Pilosocereus is one of the Cactaceae family’s most relevant genera in terms of the number of species and its wide geographical range in the Americas. Within Pilosocereus , five informal taxonomic groups have been recognized, one of which is P. leucocephalus group s.s. , whose phylogenetic relationships remain unresolved. Therefore, our objectives are to recognize the circumscriptions of the species in P. leucocephalus group s.s. and to corroborate the monophyly and phylogenetic relationships of this group through a set of morphological and molecular characters. This study is based on representative sampling along the broad distribution of this group in Mexico and Central America using multivariate and phylogenetic analyses. The morphological characters identified to contribute to species recognition and group formation are branch diameter, areole length, the areole length-width ratio, the distance between areoles, the length of the longest radial spine, and branch and spines colors. The chloroplast markers rpl16 , trnL-trnF , and petL-psbE and the nuclear marker AT1G18270 support the monophyly of the P. leucocephalus group s.s. , and two probable synapomorphies are suggested, including one transversion in rpl16 and another in petL-psbE . Together, our results demonstrate that sampled species of P. leucocephalus group s.s. encompass six species distributed in Mexico and Central America: P. alensis and P. purpusii in the western region, P. chrysacanthus and P. collinsii in the central region, and P. gaumeri and P. leucocephalus in the eastern region. A taxonomic key to recognized species is provided.
... The genetic evidence for hybridization in the cactus family was generated using different approaches and molecular markers, such as analysis of RAPD banding pattern data [10,141], levels of admixture in codominant markers (allozymes [142]; SSR [143]) and biallelic SNPs generated by RAD-Seq [27] as well as observation of reticulations in phylogenies (e.g., [13,144]). Overall, the molecular data corroborate the occurrence of interspecific hybrids in different genera, such as Opuntia [10,141], Sclerocactus [145], and Melocactus [27]. Furthermore, molecular markers have assisted studies on intergeneric hybrids in the cactus family, such as Consolea × Opuntia hybrids in the subfamily Opuntioideae [13] and Espostoa × Haageocereus in the subfamily Cactoideae [28]. ...
... Moreover, molecular markers have been useful to test taxon-specific hypotheses on species boundaries and hybridization (e.g., [143,144,146]). Interestingly, independent results have shown the maintenance of species genetic cohesion even when facing some level of genetic admixture [27,145]. For example, Khan et al. [27] investigated four hybrid zones hosting Melocactus concinnus and four congeneric species (Melocactus ernestii, Melocactus glaucescens, Melocactus paucispinus, and Melocactus zehntneri). ...
... The major role of hybridization in cactus speciation is recurrently explored in genera with high amounts of polyploids [13,14,28]. This is the case of the genus Opuntia [13,144], which presents approximately 60% of polyploid species [147]. Recently, using an integrative approach with phylogenetic, cytogenetic, and taxonomic datasets, Köhler et al. [14] showed that the octoploid (2n = 88) accessions of Opuntia aff. ...
Here, we present a review of the studies of evolutionary genetics (phylogenetics, population genetics, and phylogeography) using genetic data as well as genome scale assemblies in Cactaceae (Caryophyllales, Angiosperms), a major lineage of succulent plants with astonishing diversity on the American continent. To this end, we performed a literature survey (1992–2021) to obtain detailed information regarding key aspects of studies investigating cactus evolution. Specifically, we summarize the advances in the following aspects: molecular markers, species delimitation, phylogenetics, hybridization, biogeography, and genome assemblies. In brief, we observed substantial growth in the studies conducted with molecular markers in the past two decades. However, we found biases in taxonomic/geographic sampling and the use of traditional markers and statistical approaches. We discuss some methodological and social challenges for engaging the cactus community in genomic research. We also stressed the importance of integrative approaches, coalescent methods, and international collaboration to advance the understanding of cactus evolution.
... In Opuntia, hybridization and polyploidization is recurrently invoked as a crucial factor generating diversity (Granados-Aguilar et al., 2020;Grant & Grant, 1979;Griffith, 2001Griffith, , 2003Majure et al., 2012aMajure et al., , 2017Majure & Puente, 2014;Pinkava, 2002;Puente & Hamann, 2005;Rebman & Pinkava, 2001). Roughly 60% of the known diversity in tribe Opuntieae is polyploid (Majure et al., 2012b). ...
Hybridization plays a fundamental role in plant evolution and diversification, promoting gene flow, morphological novelties, and plant speciation. Here, we integrated fieldwork, collections-based research, morphological observations, molecular systematics, and cytogenetic data to investigate the identity of a previously unidentified taxon of Opuntia (the prickly pear cacti) observed in the north-east region of Argentina, southern South America. Our analyses revealed a cytonuclear phylogenetic discordance among nuclear and plastid genomes, as well as a polyploid nature of the studied taxon. Combining our molecular phylogenetic and cytogenetic analyses with morphological observations, we suggest that hybridization events between the native Opuntia rioplatensis and the North American introduced species, O. ficus-indica, likely produced the taxon here described as O. × cristalensis. Opuntia is the most widespread genus of Cactaceae, and many species have been introduced worldwide for an array of different purposes. Our report proposes the putative first hybridization event in Opuntia between a North American species with a southern South American lineage, which may shed light on more complex evolutionary scenarios, speciation within the group, and the impacts of species introduction.
