SciELO - Scientific Electronic Library Online

 
 número126Flora y vegetación de la región semiárida de Acultzingo-Maltrata, Veracruz, MéxicoTaxonomía, distribución geográfica y ecológica del género Penstemon (Plantaginaceae) en la Faja Volcánica Transmexicana, México índice de autoresíndice de materiabúsqueda de artículos
Home Pagelista alfabética de revistas  

Servicios Personalizados

Revista

Articulo

Indicadores

Links relacionados

  • No hay artículos similaresSimilares en SciELO

Compartir


Acta botánica mexicana

versión On-line ISSN 2448-7589versión impresa ISSN 0187-7151

Act. Bot. Mex  no.126 Pátzcuaro  2019

http://dx.doi.org/10.21829/abm126.2019.1435 

Research articles

Pollen viability and germinability of putative Bursera hybrids (section Bullockia; Burseraceae) in Mexico

Viabilidad y germinación de polen en probables híbridos de Bursera (sección Bullockia; Burseraceae) en México

Yessica Rico1  3 
http://orcid.org/0000-0002-0468-8928

Leticia Reyes-Estanislao1  2 
http://orcid.org/0000-0002-2021-6349

1Instituto de Ecología, A.C., Red de Diversidad Biológica del Occidente Mexicano, Centro Regional del Bajío, Av. Lázaro Cárdenas 253, 61600 Pátzcuaro, Michoacán, Mexico.

2Instituto Tecnológico Superior de Pátzcuaro, Ingeniería Ambiental, Av. Tecnológico 1, 61600 Pátzcuaro, Michoacán, Mexico.

Abstract:

Background and Aims:

The genus Bursera (~100 species) has its center of diversification and endemism in Mexico. Interspecific hybridization is a frequent phenomenon in Bursera in areas where related species coexist. Hybridization on the one hand can reinforce reproductive barriers, increase genetic variation, generate novel ecotypes and new lineages, and on the other hand, can lead to maladaptation. However, the ecological and evolutionary consequences of natural hybridization critically depend on hybrid fitness. In this study, within a putative hybrid population in the tropical dry forest of the Bajío region in Mexico and as a proxy of hybrid fitness, we investigated pollen viability among Bursera cuneata, B. bipinnata, and their putative hybrid.

Methods:

We used two techniques: a pollen staining test with tetrazolium chloride 1% and an in vitro germination test to observe the formation of pollen tubes. Viability percentages were calculated for each group; statistical tests were conducted with general linear models.

Key results:

Results demonstrated that the putative hybrid is not sterile and exhibited higher germination rates relative to the parental species.

Conclusions:

Our results imply that gene flow between the parental species and the putative hybrid is likely to occur. Future genetic studies should confirm the genetic identity and ploidy levels of hybrids and evaluate whether genetic introgression has occurred. Our study demonstrates that Bursera hybrids can be fertile and contributes towards understanding the role of hybridization and reproductive isolation in Mexican Bursera species.

Key words: copales; hybrid fertility; hybrid zone; in vitro germination; staining method; tropical dry forest

Resumen:

Antecedentes y Objetivos:

El género Bursera (~100 especies) tiene su centro de diversificación y endemismo en México. La hibridación interespecífica es un fenómeno común en Bursera en áreas donde coexisten especies relacionadas. La hibridación, por un lado, puede reforzar las barreras reproductivas, aumentar la variación genética, generar ecotipos novedosos y nuevos linajes y, por otro lado, puede conducir a una mala adaptación. Sin embargo, las consecuencias ecológicas y evolutivas de la hibridación natural dependen críticamente de la aptitud de los híbridos. En este estudio, dentro de una población de posibles híbridos en el bosque tropical seco de la región del Bajío en México y utilizando una aproximación de aptitud híbrida, investigamos la viabilidad del polen entre Bursera cuneata, B. bipinnata, y su respectivo híbrido hipotético.

Métodos:

Utilizamos dos técnicas: una prueba de tinción de polen con cloruro de tetrazolio 1% y una prueba de germinación in vitro para observar la formación de tubos de polen. Se calcularon porcentajes de viabilidad para cada grupo; las pruebas estadísticas se realizaron con modelos lineales generales.

Resultados clave:

Los resultados demuestran que el híbrido hipotético no es estéril y que presenta mayores tasas de germinación en comparación con las especies parentales.

Conclusiones:

Nuestros resultados sugieren que el flujo genético entre las especies parentales y el híbrido hipotético es probable. Futuros estudios genéticos deben confirmar el origen genético y nivel de poliploidía de los híbridos y determinar si existe introgresión genética. Nuestro estudio demuestra que los híbridos de Bursera pueden ser fértiles, por lo que contribuye a comprender el papel de la hibridación y el aislamiento reproductivo en las especies mexicanas de Bursera.

Palabras clave: bosque tropical caducifolio; copales; fertilidad en híbridos; germinación in vitro; técnica de tinción; zonas de hibridación

Introduction

Interspecific hybridization has important evolutionary consequences (Whitham et al., 1991), such as introduction of genetic variation into populations, generation of new ecotypes better adapted to novel environments (Pfennig et al., 2016), and development of new lineages (Abbott et al., 2013). Hybridization can also lead to maladaptation or extinction via genetic and demographic swamping (Todesco et al., 2016). Although hybridization is a widespread phenomenon in nature, it is expected that sympatric, related species develop reproductive barriers to avoid hybrid formation and maintain species integrity (Xie et al., 2017). Reproductive barriers to gene flow include prezygotic barriers that act before fertilization, preventing interspecific gene flow, and postzygotic barriers that reduce fertility of hybrids (Lowry et al., 2008; Widmer et al., 2009). For plants, prezygotic barriers include asynchrony between flowering seasons and the specificity of pollinator behavior, while an important formation of postzygotic barriers is the decrease of hybrid pollen viability, which reduces the success of backcrosses with parental species (Campbell et al., 2003; Baack et al., 2015). However, hybrids may overcome postzygotic barriers, and can be more vigorous than parental species, establishing large populations in hybrid zones (Birchler et al., 2006).

Bursera Jacq. ex L. (Burseraceae) is a diverse genus of usually deciduous shrubs and trees that comprises approximately 100 species, whose center of diversification and endemism is in the Pacific drainages of western Mexico (Rzedowski and Kruse, 1979). Bursera species are often dominant or codominant woody elements of the tropical dry forest (TDF), desert scrub and thorn scrub habitats (Miranda and Hernández-X., 1963) in Mexico (Rzedowski and Guevara-Féfer, 1992). Hybridization has been hypothesized an important process in the diversification and adaptation of Bursera (McVaugh and Rzedowski, 1965). Studies showed that natural hybridization is a frequent phenomenon in areas where closely related species co-exist (Toledo-Manzur, 1982; Rzedowski and Ortiz, 1988; Rzedowski and Guevara-Féfer, 1992; Pérez-Navarro, 2001).

Molecular and biochemical evidence has confirmed the hybrid origin of few species (Rzedowski and Ortiz, 1988; Weeks and Simpson, 2004), while field observations have noted that hybrids can be numerous and vigorous with abundant fruit production (Rzedowski and Ortiz, 1988; Rzedowski and Guevara-Féfer, 1992). So far, only one study has evaluated the reproduction of hybrids. Cortes-Palomec (1998) showed that B. medranoana Rzed. & E. Ortiz, a species of hybrid origin from B. morelensis Ramirez and B. schlechtendalii Engl., presents male infertility and thus seed production occurs through apomixis. Other genetically confirmed hybrids in the genus, B. brunea (Urb.) Urb. & Ekman and B. gracilipes Urb. & Ekman, are likely to be sterile as well (Weeks and Simpson, 2004), but no more formal studies exist.

The TDF of the Bajío region in the northeast (NE) of Michoacán and Guanajuato was one of the most widespread native habitats in this region, which at present is disappearing due to the rapid land use change towards agriculture, livestock grazing, and urbanization (Hernández-Oria, 2007). Bursera cuneata (Schltdl.) Engl. and B. bipinnata (Moc. & Sessé ex DC.) Engl. of the section Bullockia (Bridson) Razafim., Lantz & B. Bremer, known as copales, are usually codominant woody elements in the TDF in Michoacán. In rural communities, these species are used for live fences and firewood, while B. cuneata is applied for the elaboration of handicrafts. Both species have a largely allopatric distribution, but occur in sympatry in the NE of Michoacán, where field explorations of Rzedowski and Guevara-Féfer (1992) reported the presence of putative hybrids. These putative hybrids present intermediate leaf characteristics and can show abundant fruit production (Rzedowski and Guevara-Féfer, 1992).

Assessment of pollen viability among parental species and hybrids provides an easier and faster approximation to hybrid fitness relative to common-garden or breeding experiments in the field, particularly for long-lived species, such as trees (Bures et al., 2010). Pollen viability test, such as staining techniques and in vitro germination tests have widely been used to evaluate hybrid viability (Bures et al., 2010; Abdelgadir et al., 2012; García et al., 2015). Thus, the aims of this study were to evaluate whether the putative hybrid between B. cuneata and B. bipinnata is sterile, and to compare pollen viability rates among the parental species and their putative hybrid within the TDF of NE Michoacán. We expected the pollen of putative hybrids to be viable, but with lower viability and germination rates compared to those of the parental species.

Material and Methods

Study species

Bursera cuneata and B. bipinnata are dioecious and deciduous trees up to 8 m in height, with an aromatic resin, and smooth, grey bare bark (Rzedowski and Guevara-Féfer, 1992). Bursera bipinnata is distributed across the TDF of the Pacific coast from southern Chihuahua to eastern Chiapas with an altitudinal interval of 1650 to 2200 m, while B. cuneata has a smaller distribution from northeastern Michoacán and southern Guanajuato to northeastern Guerrero and south of Puebla with an altitudinal interval of 1850 to 2500 m. These species co-occur in Michoacán and Guanajuato (Rzedowski and Guevara-Féfer, 1992).

For both species, the presence of flowers occurs between May and June, while for the leaves this is between June and November; fruit production occurs from June to November and they can remain attached to the tree for long periods of time (Rzedowski and Guevara-Féfer, 1992). There are no specific studies on pollination and seed dispersal in the study region, but as in other Bursera species, they are expected to be insect-pollinated (Rzedowski and Kruse, 1979) and bird-dispersed (Ramos-Ordoñez and Arizmendi, 2011). The leaves can easily differentiate both species and the putative hybrid: B. bipinnata has bipinnate leaves, B. cuneata has larger, once-pinnate leaves, with oblong to lanceolate leaves of rugose appearance, while their putative hybrid presents intermediate morphological characteristics with partial bipinnate leaves (Figs. 1A-C).

Figure 1: Characteristic leaves of, A. Bursera cuneata (Schltdl.) Engl.; B. the putative hybrid, which presents an intermediate leave shape; C. Bursera bipinnata (Moc. & Sessé ex DC.) Engl. Scales=2 cm. 

Study site and sample collection

Field explorations during the autumn of 2017 reported a putative hybrid population with the presence of adult trees of B. bipinnata and B. cuneata and their hybrid in the TDF of the municipality Tarímbaro in Michoacán, between La Cañada del Herrero and Cañada de Los Sauces (19°43.962'N, 101°12.043'W) (Fig. 2). Rough estimates of species frequency within two TDF patches suggest that B. bipinnata, B. cuneata and their putative hybrid occur with a proportion of 6:2:1 individuals, respectively. In June 2018, when trees present both flowers and leaves that allow us to distinguish between species and the intermediate individuals, we conducted two field surveys during the mornings (9:00-11:00) to randomly collect inflorescences from male trees of each species and their putative hybrid (B. bipinnata and B. cuneata n=10 and putative hybrid n=8 trees). Inflorescences were stored in paper bags and processed in the laboratory within the same day or the following day.

Figure 2: Geographical location of the study area and sampling sites (red squares) in Tarímbaro, Michoacán, Mexico. 

Staining viability test

We used a staining method to distinguish between living and dead pollen. We prepared a solution of 0.2 g of 2, 3, 5-triphenyltetrazolium chloride (TTC) and 12 g of sucrose in 20 ml of distilled water (Norton, 1966). The TTC 1% indicates the presence of active dehydrogenase enzymes that catalyze mitochondrial respiration. We selected six fresh flowers for each individual tree collected. Pollen grains were spread on a glass slide with one drop of TTC solution, covered with a coverslip, and set aside in the dark at room temperature for 24 hr. The numbers of viable and unviable pollen grains were counted in four random optical 20× fields per slide (Primo Star LED Microscope, Carl Zeiss, Göttingen, Germany). A pollen grain was considered viable if it turned pink or red (Fig. 3A). We measured and plotted the viability of pollen for each individual as percentage, which was determined by dividing the total number of red stained pollen grains by the total number of grains observed per field.

Figure 3: A. pollen of Bursera Jacq. ex L. stained with TTC 1% at 20× and 40× optical fields, red or pink colored grain indicates a viable pollen; B. pollen tube germination colored with Toluidine blue of Bursera for the in vitro germination test at 20× and 40× optical fields, successful germination was counted when the length of the pollen tube was equal to or longer than the diameter of the grain; comparison among pollen grains for C. B. cuneata (Schltdl.) Engl.; D. the putative hybrid; E. B. bipinnata (Moc. & Sessé ex DC.) Engl. at 40× optical fields. 

In vitro germination test

Previous tests evaluated different sucrose concentrations (5, 10, 15, and 30%) on 1% agarose medium with 0.01% boric acid (H3B03) to find the most optimal pollen tube germination conditions. We found that the agarose-sucrose medium of 15% yields the highest success of pollen germination. Pollen grains from four fresh flowers per tree were evenly distributed on a glass slide with the 15% agarose-medium (0.2 cm tick) and kept in the dark at room temperature for 24 hr. To better visualize the formation of pollen tubes, a drop of Toluidine blue with 30% of glycerin solution was placed on the glass slide with a coverslip. Pollen germination was counted in four random optical 40× fields per slide (Primo Star LED Microscope, Carl Zeiss, Göttingen, Germany). A pollen grain was considered germinated when the length of the pollen tube was equal to or longer than the diameter of the grain (Fig. 3B). We estimated and plotted germination percentages for each group, which was determined by dividing the total number of germinated pollen tubes by the total number of grains observed per field.

Statistical analyses

Because data did not conform to normality assumptions even after transformation, we conducted General Linear Models (GLM) with a quasibinomial distribution to test for significant differences in the proportion of viable pollen grains among the three groups, using the glm function in R (R Core Team, 2018). The response variables were the number of viable/germination pollen grains and the number of unstained/no germinated grains per observed field. Post hoc test for pairwise comparisons were carried out by Tukey contrast with the lsmeans function in R (Lenth, 2016; R Core Team, 2018).

Results

From our pollen count observations, we did not notice apparent differences in the size of pollen grains between the putative hybrids and the parent species (Figs. 3C-E). Percentages of pollen viability for the TTC method showed that B. bipinnata presented the highest pollen viability values (46.2%, n=190 observed fields, n=10,467 observed grains), followed by B. cuneata (38.5%, n=124 observed fields, n=7625 observed grains), and the putative hybrid (36.7%, n=186 observed fields, n=10,050 observed grains) (Fig. 4A). Differences in the proportion of pollen viability through TTC were statistically significant (df=2, deviance=1015, p=0.005). Tukey post hoc comparisons revealed that B. bipinnata showed significantly higher pollen viability than the putative hybrid (p= 0.0001) and B. cuneata (p= 0.001).

Figure 4: A. total percentage of pollen viability with TTC 1%; B. in vitro germination tests, for Bursera cuneata (Schltdl.) Engl., B. bipinnata (Moc. & Sessé ex DC.) Engl., and the putative hybrid. Bars denote ± standard errors. 

For the germination test, the putative hybrid showed the highest percentage of pollen tube formation (26.9%, n=88 observed fields, n=2022 observed grains), followed by B. cuneata (23.3%, n=86 observed fields, n=2174 observed grains), and then B. bipinnata (18.2%, n=98 observed fields, n=2465 observed grains) (Fig. 4B). Differences in the proportion of pollen germination were statistically significant (df=2, deviance=35.3, p=0.0001). Post hoc comparisons revealed that the putative hybrid showed significantly higher rates of pollen tube formation than B. bipinnata (p=0.03).

Discussion

Our study represents a first test of hybridity between B. cuneata and B. bipinnata, since no genetic data are available to confirm the hybrid status of individuals with intermediate morphological characteristics. Yet, it contributes with relevant information to understand the role and consequences of hybridization in Mexican Bursera species.

The staining and in vitro germination techniques yielded good results in assessing pollen viability of Bursera species examined in this study. Both tests demonstrated that the male gametophyte in adult trees of the putative hybrid between B. cuneata and B. bipinnata is not sterile. This result contrasts with the study of Cortes-Palomec (1998), who found that the hybrid species B. medranoana is sterile. Our findings thus confirm previous field observations that suspected that Bursera hybrids can be fertile (Rzedowski and Guevara-Féfer, 1992). While some hybrids can break postzygotic barriers, it is usually expected that they present lower fertility relative to the parental species (Marques et al., 2011). We found for the staining test that the putative hybrid showed the lowest rates of pollen viability relative to both Bursera species, but the opposite was found for the in vitro germination test. Specifically, significant differences occurred between B. bipinnata and the putative hybrid, and not with respect to B. cuneata. Remarkably, the putative hybrid is morphologically more similar to B. cuneata (Fig. 1), which may imply a different degree of parental genetic background in putative hybrids.

The TTC staining technique only differentiates between living and dead pollen and is an easier technique than the in vitro germination test, as successful germination depends on finding the right medium conditions (Ilgin et al., 2007). Contrasting results between both type of techniques, as found in this study, have previously been reported in several species, and in general, it is expected that staining methods overestimate pollen viability (Nybom, 1985; Scorza and Sherman, 1995; Leila-Soares et al., 2013; Sulusoglu and Cavusoglu, 2014). Instead, in vitro germination test can yield results that better approximate the actual pollen viability, as the sucrose agar medium emulates the stigma exudate where pollen is deposited (La Porta and Roselli, 1991).

Consequences of hybridization highly depend on hybrid fitness (Todesco et al., 2016). It is usually expected that spontaneous hybrids present low fertility, but polyploid hybrid plants may have increased fertility and local adaptation respective to their diploid parental species (Alix et al., 2017). Allopolyploids are typically expected since it occurs via hybridization from the combination of divergent species of diploid genomes (Osabe et al., 2012), although autopolyploid hybrids may also occur (Barker et al., 2016). The observed higher pollen germination rate for the putative hybrid relative to at least one parent (B. bipinnata) did not follow our initial expectations. This result might be explained by the occurrence of hybrids with different genetic backgrounds, such as the formation of polyploids. Some authors argue that polyploid hybrids are characterized by a larger pollen size relative to their progenitors (Hossain et al., 1990; Wrońska-Pilarek et al., 2013, 2016), while others have found no such relationship (Franssen et al., 2001; Karlsdóttir et al., 2008; Lazarević et al., 2013). For example, Wrońska-Pilarek et al. (2013) conducted a pollen morphological comparison among three Crataegus Tourn. ex L. species, and they found that natural hybrids had larger pollen grains than the parental species, except for one species whose pollen size was similar to that of hybrids. In contrast, Franssen et al. (2001) for ten Amaranthus L. species and their interspecific hybrids, observed no differences in pollen size between hybrids and parental species, but marked differences in the number of pollen apertures. We did not observe differences in pollen size between the two Bursera species and the putative hybrids (Figs. 3C-E); however, we cannot rule out such morphological differences as we did not systematically evaluate the morphology of pollen grains. Another possibility is that the putative hybrids are not true hybrids, but only genetic data can confirm their identity.

Moreover, putative hybrids in our study site can develop vigorous adult trees with abundant number of fruits. Marques et al. (2011) found for Narcissus cavanillesii (Cav.) Barra & G. López, that F1 hybrids show high vigor at early stages of development, such as high level of growth and bulb propagation, which was explained to compensate for the low fertility of mature hybrids. In our case, it is possible that a low proportion of living pollen in the putative hybrid is compensated by a higher amount of pollen grains able to germinate. The ability of a pollen grain to grow a pollen tube is a necessary condition for fertilization. During our field collection, we observed that flowers of both Bursera species and the putative hybrid were equally visited by prospective pollinators, such as bees and wasps. This suggests that backcrosses between the parental species and the putative hybrid are likely to occur.

Pollen viability studies for TDF tree species are still scarce. Reproductive biology data present highly relevant information with consequences for species conservation and restoration. For instance, for Pachira quinata (Jacq.) W.S. Alverson fruit production was related to pollen load size, while half of the pollen grains were able to germinate and develop pollen tubes on the flower stigma (Quesada et al., 2001). Another study in Protium spruceanum (Benth.) Engl., a tree species of the Burseraceae family, showed the occurrence of high percentage (90%) of viable pollen (De Almeida-Viera et al., 2010). We found pollen viability rates below 50% for both Bursera species and the putative hybrid, which may have consequences for seed production and viability. Germination studies in Bursera species highlight low germination rates, likely due to high occurrence of empty seeds (Bonfil-Sanders et al., 2008; Hernández-Téllez, 2015). As pollen viability is only one component of fitness, future studies should contrast seed production and germination rates of parent species and their putative hybrids.

Given the frequent anecdotical observation of hybridization among Mexican Bursera species, more studies are needed to better understand the mechanisms and consequences of natural hybridization within this group. Specifically, genetic studies are required to confirm the genetic identity of putative hybrids, the maternal and paternal contribution of hybrid origin, the occurrence of diploid or polyploid hybrids, and whether several generations of hybrids coexist and if genetic introgression has occurred.

Acknowledgements

We thank the Urban Department of the H. Ayuntamiento Constitucional de Tarímbaro for the support to conduct field sampling in the municipality and Rafael Bazán for the permission to collect on his property. Sample permit SEMARNAT SGPA/DGGFS/712/1062/18. Special thanks to Bruno A. Gutiérrez Becerril and Benjamín Castillo for their field assistance. We are thankful for the comments of two anonymous reviewers that improved the quality of this work.

Literature Cited

Abbott, R., D. Albach, S. Ansell, J. W. Arntzen, S. J. E. Baird, N. Bierne, J. Boughman, A. Brelsford, C. A. Buerkle, R. Buggs, R. K. Butlin, U. Dieckmann, F. Eroukhmanoff, A. Grill, S. H. Cahan, J. S. Hermansen, G. Hewitt, A. G. Hudson, C. Jiggins, J. Jones, B. Keller, T. Marczewski, J. Mallet, P. Martinez-Rodriguez, M. Möst, S. Mullen, R. Nichols, A. W. Nolte, C. Parisod, K. Pfennig, A. M. Rice, M. G. Ritchie, B. Seifert, C. M. Smadja, R. Stelkens, J. M. Szymura, R. Väinölä, J. B. W. Wolf and D. Zinner. 2013. Hybridization and speciation. Journal of Evolutionary Biology 26(2): 229-246. DOI: https://doi.org/10.1111/j.1420-9101.2012.02599.x [ Links ]

Abdelgadir, H. A., S. D. Johnson and J. Van Staden. 2012. Pollen viability, pollen germination and pollen tube growth in the biofuel seed crop Jatropha curcas (Euphorbiaceae). South African Journal of Botany 79: 132-139. DOI: https://doi.org/10.1016/j.sajb.2011.10.005 [ Links ]

Alix, K., P. R. Gérard, T. Schwarzacher and J. S. (Pat) Heslop-Harrison. 2017. Polyploidy and interspecific hybridization: partners for adaptation, speciation and evolution in plants. Annals of Botany 120(2): 183-194. DOI: https://doi.org/10.1093/aob/mcx079 [ Links ]

Baack, E., M. C. Melo, L. H. Rieseberg and D. Ortiz-Barrientos. 2015. The origins of reproductive isolation in plants. New Phytologist 207(4): 968-984. DOI: https://doi.org/10.1111/nph.13424 [ Links ]

Barker, M. S., N. Arrigo, A. E. Baniaga, Z. Li and D. A. Levin. 2016. On the relative abundance of autopolyploids and allopolyploids. New Phytologist 210(2): 391-398. DOI: https://doi.org/10.1111/nph.1369 [ Links ]

Birchler, J. A., H. Yao and S. Chudalayandi. 2006. Unraveling the genetic basis of hybrid vigor. Proceedings of the National Academy of Sciences of the United States of America 103(35): 12957-12958. DOI: https://doi.org/10.1073/pnas.0605627103 [ Links ]

Bonfil-Sanders, C., I. Cajero-Lázaro and R. Y. Evans. 2008. Germinación de semillas de seis especies de Bursera del centro de México. Agrociencia 42(7): 827-834. [ Links ]

Bures, P., P. Smarda, O. Rotreklova, M. Oberreiter, M. Buresova, A. Knoll, K. Fajmon and J. Smerda. 2010. Pollen viability and natural hybridization of Central European species of Cirsium. Preslia 82(4): 391-422. [ Links ]

Campbell, D. R., R. Alarcon and C. A. Wu. 2003. Reproductive isolation and hybrid pollen disadvantage in Ipomopsis. Journal of Evolutionary Biology 16(3): 536-540. DOI: https://doi.org/10.1046/j.1420-9101.2003.00538.x [ Links ]

Cortes-Palomec, A. C. 1998. Biología reproductiva de Bursera medranoana Rzedowski & Ortiz (Burseraceae). Una especie de origen híbrido. Tesis de licenciatura. Facultad de Ciencias, Universidad Nacional Autonoma de México. México, D.F., México. 59 pp. [ Links ]

De Almeida-Vieira, F., V. Appolinario, C. Gouvea-Fajardo and D. De-Carvalho. 2010. Reproductive biology of Protium spruceanum (Burseraceae), a dominant dioecious tree in vegetation corridors in Southeastern Brazil. Revista Brasileira de Botânica 33(4): 711-715. DOI: https://dx.doi.org/10.1590/S0100-84042010000400018 [ Links ]

Franssen, A. S., D. Z. Skinner, K. Al-Khatib and M. J. Horak. 2001. Pollen morphological differences in Amaranthus species and interspecific hybrids. Weed Science 49(6): 732-737. DOI: https://doi.org/10.1614/0043-1745(2001)049[0732:PMDIAS]2.0.CO;2 [ Links ]

García, L., M. Rivero and F. Droppelmann. 2015. Descripción morfológica y viabilidad del polen de Nothofagus nervosa (Nothofagaceae). BOSQUE 36(3): 487-496. DOI: https://dx.doi.org/10.4067/S0717-92002015000300015 [ Links ]

Hernández-Oria, J. G. 2007. Desaparición del bosque seco en el Bajío mexicano: implicaciones del ensamblaje de especies y grupos funcionales en la dinámica de una vegetación amenazada. Zonas Áridas 11(1): 13-31 DOI: https://dx.doi.org/10.21704/za.v11i1.201 [ Links ]

Hernández-Téllez, I. J. 2015. Viabilidad y germinación de diez especies del género Bursera. Tesis de licenciatura. Facultad de Ciencias, Universidad Nacional Autónoma de México. México, D.F., México. 72 pp. [ Links ]

Hossain, M. M., H. Inden and T. Asahira. 1990. Pollen morphology of interspecific hybrids of Brassica oleracea and B. campestris. HORTSCIENCE 25(1): 109-111. [ Links ]

Ilgin, M., F. Ergenoglu and S. Caglar. 2007. Viability, germination and amount of pollen in selected caprifig types. Pakistan Journal of Botany 39(1): 9-14. [ Links ]

Karlsdóttir, L., M. Hallsdóttir, A. T. Thórsson and K. Anamthawat-Jónsson. 2008. Characteristics of pollen from natural triploid Betula hybrids. Grana 47(1): 52-59. DOI: https://doi.org/10.1080/00173130801927498 [ Links ]

La Porta, N. and G. Roselli. 1991. Relationship between pollen germination in vitro and fluorochromatic reaction in cherry clone F12/1 (Prunus avium L.) and some of its mutants. Journal Horticultural Science and Biotechnology 66(2): 171-175. DOI: https://doi.org/10.1080/00221589.1991.11516141 [ Links ]

Lazarević, M., S. Siljak-Yakovlev, P. Lazarević, B. Stevanović and V. Stevanović. 2013. Pollen and seed morphology of resurrection plants from the genus Ramonda (Gesneriaceae): relationship with ploidy level and relevance to their ecology and identification. Turkish Journal of Botany 37(5): 872-885. DOI: https://doi.org/10.3906/bot-1209-58 [ Links ]

Leila-Soares, T., O. De Nunes Jesus, J. Almeida Dos Santos-Serejo and E. De Jorge Oliveira. 2013. In vitro pollen germination and pollen viability in passion fruit (Passiflora spp.). Revista Brasileira de Fruticultura 35(4): 1116-1126. DOI: https://dx.doi.org/10.1590/S0100-29452013000400023 [ Links ]

Lenth, R. V. 2016. Least-Squares Means: The R Package lsmeans. Journal of Statistical Software 69(1): 1-33. DOI: https://doi.org/10.18637/jss.v069.i01 [ Links ]

Lowry, D. B., J. L. Modliszewski, K. M. Wright, C. A. Wu and J. H. Willis. 2008. The strength and genetic basis of reproductive isolating barriers in flowering plants. Philosophical Transactions of the Royal Society of London, Series B, Biological Sciences 363(1506): 3009-3021. DOI: https://doi.org/10.1098/rstb.2008.0064 [ Links ]

Marques, I., G. N. Feliner, M. Ameíia, M.-L. Louçaõ and J. F. Aguilar. 2011. Fitness in Narcissus hybrids: low fertility is overcome by early hybrid vigour, absence of exogenous selection and high bulb propagation. Journal of Ecology 99(6): 1508-1519. DOI: https://doi.org/10.1111/j.1365-2745.2011.01876.x [ Links ]

McVaugh, R. and J. Rzedowski. 1965. Synopsis of the genus Bursera L in western Mexico, with notes on the material of Bursera collected by Sessé and Mociño. Kew Bulletin 18(2): 317-346. DOI: https://doi.org/10.2307/4109252 [ Links ]

Miranda, F. and E. Hernández-X. 1963. Los tipos de vegetación en México y su clasificación. Boletín de la Sociedad Botánica de México 28: 29-179. DOI: https://dx.doi.org/10.17129/botsci.1084 [ Links ]

Norton, J. D. 1966. Testing of plum pollen viability with tetrazolium salts. Proceedings of the American Society for Horticultural Science 89: 132-134. [ Links ]

Nybom, H. 1985. Pollen viability assessments in blackberries (Rubus subgen. Rubus). Plant Systematics and Evolution 150(3): 281-290. DOI: https://doi.org/10.1007/BF00984202 [ Links ]

Osabe, K., T. Kawanabe, T. Sasaki, R. Ishikawa, K. Okazaki, E. S. Dennis, T. Kazama and R. Fujimoto. 2012. Multiple mechanisms and challenges for the application of allopolyploidy in plants. International Journal of Molecular Sciences 13(7): 8696-8721. DOI: https://doi.org/10.3390/ijms13078696 [ Links ]

Pérez-Navarro, J. J. 2001. El género Bursera Jacq. ex L. (Burseraceae) en la Península de Baja California. Tesis de maestría. Centro de Investigaciones Biológicas del Noroeste, S.C. La Paz, Baja California, México. 110 pp. [ Links ]

Pfennig, K. S., A. L. Kelly and A. A. Pierce. 2016. Hybridization as a facilitator of species range expansion. Proceedings Biological Sciences 283(1839): 20161329 DOI: https://doi.org/10.1098/rspb.2016.1329 [ Links ]

Quesada, M., E. J. Fuchs and J. A. Lobo. 2001. Pollen load size, reproductive success, and progeny kinship of naturally pollinated flowers of the tropical dry forest tree Pachira quinata (Bombacaceae). American Journal of Botany 88(11): 2113-2118. DOI: https://doi.org/10.2307/3558436 [ Links ]

R Core Team. 2018. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. [ Links ]

Ramos-Ordoñez, M. and M. Arizmendi. 2011. Parthenocarpy, attractiveness and seed predation by birds in Bursera morelensis. Journal of Arid Environments 75(9): 757-762. DOI: https://doi.org/10.1016/j.jaridenv.2011.04.013 [ Links ]

Rzedowski, J. and E. Ortiz. 1988. Estudios quimiotaxonómicos de Bursera (Burseraceae). II. Una especie nueva de origen hibrido de la Barranca de Tolantongo, estado de Hidalgo. Acta Botanica Mexicana 1: 11-19. DOI: https://doi.org/10.21829/abm1.1988.559 [ Links ]

Rzedowski, J. and F. Guevara-Féfer. 1992. Burseraceae. Flora del Bajío y de regiones adyacentes 3: 1-46. [ Links ]

Rzedowski, J. and H. Kruse. 1979. Algunas tendencias evolutivas en Bursera (Burseraceae). Taxon 28(1-3): 103-116. DOI: https://doi.org/10.2307/1219565 [ Links ]

Scorza, R. and W. B. Sherman. 1995. Peaches. In: Janik, J. and J. N. Moore (eds.). Fruit breeding. John & Sons. New York, USA. Pp. 325-440. [ Links ]

Sulusoglu, M. and A. Cavusoglu. 2014. In vitro pollen viability and pollen germination in cherry laurel (Prunus laurocerasus L.). The Scientific World Journal 2014: 657123. DOI: https://dx.doi.org/10.1155/2014/657123 [ Links ]

Todesco, M., M. A. Pascual, G. L. Owens, K. L. Ostevik, B. T. Moyers, S. Hübner, S. M. Heredia, M. A. Hahn, C. Caseys, D. G. Bock and L. H. Rieseberg. 2016. Hybridization and extinction. Evolutionary Applications 9(7): 892-908. DOI: https://doi.org/10.1111/eva.12367 [ Links ]

Toledo-Manzur, C. A. 1982. El género Bursera (Burseraceae) en el estado de Guerrero (Mexico). Tesis de licenciatura. Facultad de Ciencias, Universidad Nacional Autónoma de Mexico. México, D.F., México. 364 pp. [ Links ]

Weeks, A. and B. B. Simpson. 2004. Molecular genetic evidence for interspecific hybridization among endemic Hispaniolan Bursera (Burseraceae). American Journal of Botany 91(6): 976-984. DOI: https://doi.org/10.3732/ajb.91.6.976 [ Links ]

Whitham, T., P. Morrow and B. Potts. 1991. Conservation of hybrid plants. Science 254(5033): 779-780. DOI: https://doi.org/10.1126/science.254.5033.779-b [ Links ]

Widmer, A., C. Lexer and S. Cozzolino. 2009. Evolution of reproductive isolation in plants. Heredity 102(1): 31-38. DOI: https://doi.org/10.1038/hdy.2008.69 [ Links ]

Wrońska-Pilarek, D., J. Bocianowski and A. M. Jagodziński. 2013. Comparison of pollen grain morphological features of selected species of the genus Crataegus (Rosaceae) and their spontaneous hybrids. Botanical Journal of the Linnean Society 172(4): 555-571. DOI: https://doi.org/10.1111/boj.12033 [ Links ]

Wrońska-Pilarek, D. , W. Danielewicz, J. Bocianowski, T. Maliński and M. Janyszek. 2016. Comparative Pollen Morphological Analysis and Its Systematic Implications on Three European Oak (Quercus L., Fagaceae) Species and their spontaneous hybrids. PloS ONE 11(8): e0161762. DOI: https://doi.org/10.1371/journal.pone.0161762 [ Links ]

Xie, Y., X. Zhu, Y. Ma, J. Zhao, L. Li and Q. Li. 2017. Natural hybridization and reproductive isolation between two Primula species. Journal of Integrative Plant Biology 59(8): 526-530. DOI: https://doi.org/10.1111/jipb.12546 [ Links ]

Author contributions

YR conceived and designed the study. LRE and YR conducted the field sampling and laboratory procedures. YR analyzed the data and wrote the manuscript. LRE carefully revised the manuscript.

Funding

This study was funded by Consejo Nacional de Ciencia y Tecnología (CONACYT) Ciencia Básica project I0017-283237.

To cite as:

Rico, Y. and L. Reyes-Estanislao. 2018(2019). Pollen viability and germinability of putative Bursera hybrids (section Bullockia; Burseraceae) in Mexico. Acta Botanica Mexicana 126: e1435. DOI: 10.21829/abm126.2019.1435

Received: August 06, 2018; Accepted: October 17, 2018

3Author for correspondence: yessica.ricom@gmail.com

Creative Commons License Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons