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Article

Genetic Diversity in Sporophytic Apomictic Neotropical Savanna Trees: Insights from Eriotheca and Handroanthus Agamic Complexes

by
Rafaela Cabral Marinho
1,2,*,
Mariana Gonçalves Mendes
3,
Clesnan Mendes-Rodrigues
4,
Ana Maria Bonetti
3,
Eduardo Leite Borba
5,
Paulo Eugênio Oliveira
1 and
Diana Salles Sampaio
1
1
Institute of Biology, Federal University of Uberlândia (UFU), Uberlândia 38408-100, Minas Gerais, Brazil
2
Academic Institute of Health and Biological Sciences, State University of Goiás, Itumbiara 75536-100, Goiás, Brazil
3
Instituto de Biotecnologia, Federal University of Uberlândia (UFU), Uberlândia 38408-100, Minas Gerais, Brazil
4
Faculty of Medicine, Federal University of Uberlândia, Uberlândia 38408-100, Minas Gerais, Brazil
5
Department of Botany, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte 31270-901, Minas Gerais, Brazil
*
Author to whom correspondence should be addressed.
Diversity 2025, 17(4), 254; https://doi.org/10.3390/d17040254
Submission received: 28 January 2025 / Revised: 2 March 2025 / Accepted: 4 March 2025 / Published: 31 March 2025
(This article belongs to the Section Plant Diversity)
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Abstract

:
Apomictic populations, which produce seeds with embryos without proper sexual syngamy, often show low genetic diversity, but eventually, such diversity has been reported to be surprisingly high. We studied here the genetic diversity in agamic complexes of Eriotheca crenulata (comb. n. E. gracilipes), E. pubescens (Malvaceae-Bombacoideae), and Handroanthus ochraceus (Bignoniaceae), tropical tree species from the savannas in Central Brazil. We evaluated the genetic diversity and structure of self-fertile polyploid sporophytic apomicts versus self-sterile diploid or tetraploid sexual populations by using dominant ISSR markers. Genetic diversity was either similar or even higher in apomictic populations of E. crenulata and E. pubescens, but the opposite was observed in some populations of H. ochraceus. Only two individuals of E. pubescens showed identical ISSR profiles, so strict clonality in adult individuals was very rare among the studied trees. The genetic variability was notably higher within populations than among populations of H. ochraceus and very similar among and within populations of Eriotheca species. Ordination, clustering, and Bayesian analyses showed a clear distinction between populations of Eriotheca species with different breeding systems. But for H. ochraceus, a sexual population was actually grouped with the apomictics. As in other studies, eventual sexual and recombination events seem to increase genetic diversity in apomictic populations. This may explain the similar genetic diversity among apomictic and sexual populations in the studied agamic complexes and the virtual absence of strict clonal individuals. The results have evolutionary and ecological consequences for the threatened Neotropical savanna trees.

1. Introduction

Apomixis, the formation of embryos inside seeds without proper sexual syngamy, may lead to the development of embryos from nonreduced embryo sac cells (gametophytic apomixis) or even lead to the development of embryos from sporophyte mother’s tissue cells (sporophytic apomixis) [1,2]. Therefore, apomicts are supposed to be genetically similar, and populations putatively show low genetic variation, especially in gametophytic obligate apomicts e.g., [3], which are mostly herbs from temperate environments, historically the most studied group of apomicts [4]. However, many tropical species are sporophytic apomicts, with apomixis as a reproductive alternative, occurring together with sexual events and leading to agamic complexes with mixed breeding systems [5,6,7,8,9,10,11]. Population genetics studies with apomict tropical tree species and sporophytic apomicts are scarce, so the level of genetic similarities within these populations is an open area for new investigations.
Studies based on molecular markers have revealed that there is considerable genetic diversity in gametophytic apomictic populations [9,12,13,14]. The genetic variability among apomicts is usually attributed to factors such as high heterozygosity derived from polyploidization and the coexistence of apomixis and sexual reproduction (facultative apomixis) [15,16]. Facultative apomixis is common in sporophytic apomictic species, which often depend on proper fertilization to produce an endosperm, a process referred as pseudogamy [2,4]. In these cases, the pollen tube penetrates the embryo sac, and the egg cell can also be fertilized, giving rise to a zygotic embryo [1]. Thus, multiple adventitious embryos can develop concomitantly with the sexual one, originating polyembryonic seeds of mixed origin [17]. Facultative apomixis, with polyembryonic seeds of mixed origin, can also be found less often in some aposporous gametophytic apomicts, in which a nonreduced embryo sac may coexist with a reduced one, although most often only one develops into one seed [7]. Nevertheless, in diplospory, another kind of gametophytic apomixis, the embryo originates mostly from nonreduced gametophyte/embryo sac elements, and apomixis is often autonomous [1,8]. But even in these later cases, apomicts may reveal distinct and unique genotypes [9,13,14], which may arise due to recombination, mutations, or chromosome re-arrangements [2,6,9,12]. Thus, besides the reproductive assurance, apomicts may associate it with the advantages of seed dispersal, retaining the level of heterozygosity, and preserving and disseminating locally adapted genotypes [18].
Based on the occurrence of neopolyploidy and high rates of polyembryony, usually associated with apomixis, agamic complexes have been detected for some groups of woody plants in Cerrado, the Neotropical savannas in Central Brazil [11,19,20]. Some of the most representative agamic complexes in Cerrado belong to the Bignoniaceae [19,20,21] and Malvaceae [11]. Both Malvaceae (especially in Bombacoideae) and Bignoniaceae present predominantly sexual self-incompatible species [11,22], but many sporophytic apomictic self-compatible populations have been described [11,20,21,23]. In this sense, those apomictic plants need active pollination to set fruits and seeds [11,23], and histological analyses indicate the presence of sexual embryos coexisting with adventitious ones [17,21]. But to what extent this coexistence influences the genetic diversity of apomicts versus sexual individuals or populations is yet to be defined.
We studied three agamic complexes of Cerrado trees. Eriotheca crenulata (K. Schum.) Yoshikawa and M.C. Duarte (comb. n. E. gracilipes) and Eriotheca pubescens (Mart. and Zucc.) Schott and Endl (Malvaceae-Bombacoideae) are widely distributed tree species in Cerrado with both sexual/diploid or tetraploid populations and apomictic/hexaploid ones [24]. A third complex, Handroanthus ochraceus (Cham.) Mattos (Bignoniaceae) is a widespread small tree in open Cerrado areas with sexual/diploid and apomictic/tetraploid populations [20].
We evaluated the genetic diversity of apomictic versus sexual populations of E. crenulata, E. pubescens, and H. ochraceus using ISSR dominant markers (Inter Simple Sequence Repeats). ISSR markers are effective for studying the genetic diversity of polyploid plant populations due to their compatibility with the genomic complexity of these organisms. In polyploid plants, the presence of multiple chromosome sets complicates allele differentiation when using codominant markers such as SSRs, which, in this context, must often be treated as dominant, preventing the accurate assessment of heterozygosity [2]. Although the primary advantage of ISSR over SSRs lies in their broad applicability without requiring prior genomic information, as ISSR markers are less influenced by ploidy variations, they have been used in recent genetic diversity studies, linkage mapping, and germplasm conservation of ploidy complexes [25,26]. Moreover, with due care, ISSR markers offer high reproducibility and informativeness, generating a significant number of polymorphic bands that enable robust genetic diversity analyses even in complex genomes (e.g., [14]).
In this sense, we aimed to verify (1) whether the genetic diversity is distinct between populations with contrasting breeding systems, (2) if apomixis leads to a higher number of shared loci and clonality, and (3) whether differences among populations lead to clustering and genetic structuring.

2. Methods

2.1. Biological Material

Leaf samples were collected from 2010 to 2012. The embryonic pattern and ploidy level were described for all populations in previous studies [11,17,20,24,27]. We studied 36 individuals from two populations (one apomictic and one sexual) of Eriotheca crenulata, 38 individuals from two populations (one apomictic and one sexual) of E. pubescens, and 117 individuals from six populations (three apomictic and three sexual) of H. ochraceus (Figure 1, Table 1). For all studied plants, immediately after collection, leaves were stored in silica gel until extraction of the genomic DNA.
All populations were consistently either apomictic, polyembryonic, and polyploid (tetraploid for Handroanthus or hexaploid for Eriotheca) or sexual, monoembryonic, and with lower ploidy levels (either diploid for Handroanthus or tetraploid for Eriotheca). But one of them (H. ochraceus, Córrego D’anta—MG—HOA1, see Table 1), despite all individuals showing tetraploidy and high rates of polyembryony (27–66% [27]), included a diploid individual with 2% of polyembryonic seeds [20]. The difference in the number of populations studied for the two genera can be explained by the greater difficulty encountered in extracting good-quality DNA for the amplification of Eriotheca species. Eriotheca leaves have a large amount of mucilaginous substances and numerous trichomes that make extraction and amplification difficult.

2.2. DNA Extraction and ISSR-PCR

DNA extraction was performed using the DNeasy® Plant mini extraction kit (Qiagen, Hilden, Germany), following the manufacturer’s recommendations. Among the ISSR primers initially tested for the species, 10 were chosen for each species based on the larger number of polymorphic bands obtained. The annealing temperatures of the primers were optimized for each ISSR locus (Supporting Information Table S1). Each selected primer was used for three separate PCR (polymerase chain reaction) amplifications to allow us to compare gel photographs (see Supporting Information Figure S1 for examples of gel quality) and avoid reproducibility problems described for the technique [28].
The final volume of the working solution for each reaction was 19 μL, with 2.0 μL of 10× Buffer, 0.21 mM dNTP, 0.32 μM primer, 1 U Taq polymerase (Sigma, St. Louis, MI, USA), using 10–20 ng DNA template, and Milli-Q (Millipore, 161 Burlington, MA, USA) ultrapure water. Amplifications were performed on Gene Amp System 9700 (Applied Biosystems) and Arktik Thermal Cycler (Thermo Fisher Scientific, Vantaa, Finland) thermocyclers. For PCR, the samples were subjected to the temperature of 94 °C for 4 min for denaturation, followed by 37 cycles of amplification: 94 °C for 1 min for denaturation, 2 min for annealing, where the annealing temperatures varied according to the primer (Supporting Information Table S1), 72 °C for 2 min for extension, and final extension at 72 °C for 7 min. The amplification products were separated by agarose gel electrophoresis (1.5%), stained with ethidium bromide (0.5 mg/mL), and immersed in 0.5× TBE (0.2 M Tris base, 0.5 M boric acid, 5 mM EDTA) at 80 volts for 3 h and photographed under ultraviolet light in Image Quant 150 transilluminator (GE Healthcare UK Ltd., Little Chalfont, UK). A molecular ladder of 100 pb was used to follow the electrophoretic separation and to estimate the size of the obtained fragments.

2.3. Data Analyses

The fragments obtained by amplification were evaluated for presence (1) and absence (0), producing a binary matrix. Non-specific bands were discarded from the analyses. As mentioned earlier, we used the replicas of the gels for each primer to avoid scoring non-specific bands or failing to score specific ones. GeneAlex 6.41 [29] was used to obtain diversity indexes, such as the percentage of polymorphic bands (P), Shannon index (I), expected heterozygosity (He), Nei’s unbiased genetic distance and genetic distance between individuals (GD). For each population, genetic diversity indexes, I and He, were contrasted using a 95% confidence interval (95%CI). Non-overlapping 95%CI between populations for each pairwise indicated differences in genetic diversity. The Multilocus Matches analyses (GenAlEx 6.41) were carried out for each population to assess the presence of pairs of individuals with identical loci and the number of loci that differed among individuals. A Mantel test (also in GenAlEx 6.41) was performed to verify if there was a significant correlation between genetic and spatial distance among populations. Principal coordinate analyses (PCoA) were carried out using GenAlEx GD matrices, and the resulting data were organized as 3-D plots using the rgl and plot3D packages in the R environment [30,31], which were redrawn by hand afterward to show the population on the Axis 1 and Axis 2 plane. The PCoA analysis was undertaken for the Eriotheca species together.
Analyzes of molecular variance (AMOVA) were performed, also using GeneAlex 6.41, among and within populations for each Eriotheca species separately. For H. ochraceus, a first AMOVA was carried out to test the variance among and within populations, a second considering sexual and apomictic as different groups, and a third considering the groups formed after the Bayesian analysis.
The AFLP-SURV program [32] was used to generate matrices of dissimilarity, considering the Bayesian method with 100 permutations and 1000 bootstraps. The PHYLIP 3.69 application [33] was used to construct 1000 dendrograms using the neighbor-joining algorithm. Neighbor-joining consensus trees with respective boostrap values were produced using the CONSENSE package of the same application. The neighbor-joining dendrogram was elaborated for both Eriotheca species together.
A further Bayesian analysis was carried out in the STRUCTURE 2.2 program [34] to determine the number of genetic groups (K) and to identify patterns of genetic structuring in the species. The number of genetic groups tested ranged from K = 1 to K = 6 for Eriotheca (both species were analyzed together and then separately) and K = 1 to K = 7 for Handroanthus, with 15 runs corresponding to each K. Each run had 1,000,000 Monte Carlo Markov chain iterations (MCMC) with 100,000 initial iterations (burn-in). The admixture model and correlated allele frequencies were adopted. In order to define the best K, the Harvest program was used. To infer the number of clusters or presumed populations, the mean of each probability value K, the “probability log” (ln P(D)), was calculated across all runs, we also calculated the statistical delta of K (ΔK) [35].

3. Results

The ten ISSR primers selected for the study generated 111 fragments for Eriotheca and 104 fragments for Handroanthus. Some analyses of genetic diversity were made independently for E. crenulata using 99 fragments and for E. pubescens using 80 fragments, as described below. The percentage of polymorphic bands (P), Shannon index (I), and expected heterozygosity (He) were not different between apomictic and sexual populations of E. crenulata (means of I = 0.363 and He = 0.251 for apomictic and I = 0.294 and He = 0.201 for sexual individuals). Overlapping 95% confidence interval and similar genetic diversity indexes were also observed for E. pubescens sexual and apomictic populations (means of I = 0.396 and He = 0.271 for apomictic and I = 0.396 and He = 0.273 for sexual individuals). However, the indexes were significantly higher in some of the sexual populations of H. ochraceus, although differences were not markedly large (means of I = 0.373 and He = 0.249 for sexual and I = 0.308 and He = 0.205 for apomictic individuals). See detailed results in Table 2.
In the multiloci genotypes analyses performed for E. crenulata, the pairs of loci in sexual individuals differed between 3 and 27 loci and in apomicts ones between 2 and 27. For E. pubescens, in sexual individuals, the pairs of loci differed between 6 and 25, and in apomicts, ones between 0 and 26. Only one pair of individuals did present identical ISSR profiles. For H. ochraceus, the pairs of individuals in sexual populations differed between 13 and 46 loci and in apomictic populations between 10 and 42 loci (Table 2), and no individuals presented identical ISSR profiles.
The main coordinate analysis PCoA for Eriotheca showed that 64.36% of the variation was explained by the first axis, 14.09% by the second, and 12.13% by the third axis. Such analysis clearly separated the Eriotheca species and the populations within each species with no overlap (Figure 2A). In the PCoA for H. ochraceus 33.81% of the variation was explained by the first axis, 19.35% by the second, and 18.17% by the third axis. The analysis clearly separated the two sexual populations (HOS2 and HOS3) from the others (Figure 3A). The PCoA also separated an apomictic population (HOA2) from the other apomictic populations (HOA1 and HOA3) and the sexual population HOS1. The populations HOS1, HOA1, and HOA3 overlapped and were not clearly distinguished by the PCoA.
In the AMOVA analyses, the percentage of variation within and among populations was similar (varying from 47% to 53%) in the two species of Eriotheca. However, in E. crenulata the greatest variation was found among populations with different breeding systems, and in E. pubescens, the greatest variation was found within populations (Table 3). The AMOVA analyses performed for H. ochraceus showed that the highest percentage of variation occurred within populations (61%) (Table 3). In the AMOVA performed with the populations of H. ochraceus grouped after Bayesian analysis, the variation between groups was 12%, contrasting with the 1% found when comparing populations grouped by distinct breeding systems. Again, the highest percentage of variation (58%) occurred within populations of each Bayesian group (Table 3).
The neighbor-joining dendrogram for Eriotheca grouped together conspecific populations with bootstrap support lower than 50% (Figure 2B). For H. ochraceus, the dendrogram formed two main groups, one with the sexual HOS2 and HOS3, with bootstrap support lower than 50%, and another with the apomictic populations and the sexual HOS1 with bootstrap support of 86%. In addition, the dendrogram showed the apomictic HOA2 distinct from the rest of the group (HOA1, HOA3, and HOS1) with bootstrap support of 59% (Figure 3B).
The Bayesian analyses basically reflected the relationships observed in the Neighbor-joining dendrogram. In the structure Bayesian analysis for Eriotheca, the best K value was 2 (Figure 2C,D), separating the two Eriotheca species and grouping the populations of each species (Figure 2G). However, when the analysis was carried out for each species separately, the sexual and apomictic populations appeared distinct (Figure 2E,F), concurring with PCoA results (Figure 2A). In Bayesian analysis for H. ochraceus, the best K value was also 2 (Figure 3C,D), supporting a group with the sexual HOS2 and HOS3 and another group with the apomictic populations (HOA1, HOA2, and HOA3) together with HOS1 (Figure 3C). Admixture was very limited, indicating a low genetic flow among groups. Although neighbor-joining and the Bayesian analyses showed distinct genetic groups in the studied agamic complexes, there was no significant correlation between genetic and spatial distance according to the Mantel test for either studied group (Eriotheca species, p = 0.59; H. ochraceus, p = 0.51).

4. Discussion

The results obtained here showed that the genetic diversity of apomictic populations was not markedly different from the sexual ones in the agamic complexes studied. Contrary to expectations, eventually, the genetic diversity was even slightly higher in apomictic populations than in conspecific sexual ones, as in Eriotheca species. The diversity is possibly the result of sexual events in the sporophytic apomictic populations. Population diversity was always high enough to make strict clonality rare, even estimated by the ISSR dominant markers used here. Below, we discuss these trends in detail and consider the ecological and evolutionary consequences of these findings.

4.1. Genetic Diversity in Apomictic vs. Sexual Populations

Theoretically, in sporophytic apomictic populations, individuals originated from adventitious embryos, and their mother plants would be genetically identical [2,36]. Although apomictic populations of Eriotheca species and H. ochraceus showed high rates of polyembryonic seeds [11,20], which would imply at least one adventitious embryo per seed [17], only one pair of adult individuals was identical, in an apomictic E. pubescens population, based on multiloci genotypes analysis of the ISSR markers. Previous studies with RAPD markers for an apomictic population of E. pubescens also indicated high variability but identified more potentially clonal individuals [37].
The absence or small number of strictly clonal individuals in these agamic complexes is surprising, especially since ISSR dominant markers, despite being less affected by the ploidy differences [24], tend to underestimate genetic differences. However, strict clonal lineages are really rarer in nature. In Paspalum, for example, autotetraploid apomictics are of multiple independent origins, with a single effective clonal genotype and other genotypes diversified by sexual recombination [38]. Even pollen sterile and obligatory diplosporic apomicts, such as Cerrado Miconia albicans (Melastomataceae), present almost no strict clonal lineages [13,14].
The high genetic diversity found here within apomictic populations can be explained primarily by facultative events of sexuality in sporophytic apomicts populations [39]. Mutations, as described for gametophytic apomicts [13,14], were possibly less important. In the studied species, adventitious embryo development and seed formation rely on endosperm formation, which depends on pollen tube growth and fertilization and may generate sexual embryos and mixed mating [17,20]. Although a mixed mating is inferred for apomictic populations of these species, the greater genetic variation found within populations in AMOVA analysis corresponds to typical allogamous populations [40] and indicates the preponderance of cross-fertilization during the sexual events or further natural selection of allogamous individuals. In this sense, facultative apomixis would allow the concomitant occurrence of clones originated by adventitious embryos together with new genotypes arising from sexual events, a kind of “best of both worlds” strategy described elsewhere (e.g., [41]).

4.2. Evolutionary and Ecological Implications of Facultative Apomixis

Analyzing the diversity indices (P, I, and He), E. crenulata showed slightly higher diversity in the apomictic population than in the sexual ones. Meanwhile, in E. pubescens, the diversity indices were very similar between apomictic and sexual populations. Generalizations about the genetic diversity of the studied Eriotheca species are difficult because there are no other studies of genetic diversity within the genus. Studies with the related Bombacoideae, such as Adansonia digitata L., the self-incompatible and tetraploid Baobab species [42], and Ceiba pentandra (L.) Gaertn, a self-incompatible and diploid large rainforest tree [43,44], shows high levels of genetic diversity when analyzed with microsatellite markers, He= 0.712 to 0.811 [45], and He = 0.814 to 0.895 [46]. Although such indexes cannot be directly compared with the obtained here to Eriotheca, such codominant markers can show genetic diversity commonly three times higher than the obtained with dominant markers such as ISSR [40].
Analyzing the diversity indices (P, I, and He) in H. ochraceus, it shows higher levels of genetic diversity in some of the sexual populations than in the apomictic ones. But even in this case, genetic diversity levels were not markedly different. In Bignoniaceae, the studies made using other markers did not consider the ploidy and the embryonic pattern of the species. There are no data for H. ochraceus with dominant markers; however, the percentage of polymorphic bands in sexual populations of H. ochraceus (p = 73.8%) was similar to the obtained from the self-incompatible Bignoniaceae Jacaranda decurrens Cham. with RAPD dominant markers (p = 69.2%) [47]. In addition, the percentage of polymorphic bands found for apomictic populations in the present study (p = 59.62%) was lower than the observed for the apomictic self-fertile Bignoniaceae Anemopaegma arvense (Vell) Stellf. ex de Souza (p = 72.8%) with dominant RAPD markers [48].
Handroanthus ochraceus apomictic populations showed higher genetic diversity within populations than among populations, as found for the apomictic self-fertile A. arvense, Bignoniaceae, (71.72%, with RAPD markers) [48] and for the self-sterile J. decurrens, also Bignoniaceae, (ca. 70% with RAPD and AFLP markers) [47]. This supports the idea that the sporophytic apomictic Bignoniaceae population structure is similar self-sterile species. These results contrast with the self-fertile Incarvillea younghusbandii Sprague, Bignoniaceae, which sports higher genetic diversity among populations (61%; AFLP) [49], as does gametophytic apomictic Ranunculus carpaticola Soó, Ranunculaceae (56.68%; AFLP) (9); and Miconia albicans (Sw.) Triana, Melastomataceae, (74%; ISSR) [13].
The genetic structure of sexual and apomictic populations was clearly differentiated by PCoA of Eriotheca species and by PCoA, neighbor-joining dendrogram, and Bayesian analyses of genetic diversity for H. ochraceus. However, a sexual population of H. ochraceus in Uberlândia-MG (HOS1) was grouped with the apomictic populations in these analyses, which was reinforced by the results of AMOVA that show variation between a group of sexual populations (HOS2 and HOS3) and another group of apomictic populations (HOA1, HOA2, and HOA3) together with the sexual HOS1 population, indicating an important differentiation between them. This link between the apomictic and the sexual Handroanthus suggests a common origin and/or persistent gene flow among sexual diploid and apomictic polyploid populations, as observed elsewhere [50].

4.3. General Considerations

Our general findings on the genetic structure of agamic complexes are similar to other sporophytic apomictic Cerrado species and corroborate facultative apomixis. A recent study with Zygopetalum mackayi (Orchidaceae), which, in addition to using ISSR markers, also used SSR codominant markers, showed only two individuals with identical genotypes and high levels of genetic diversity for this perennial herb [39].
This strategy of facultative apomixis seems to have been important in a scenario of Pleistocene climate fluctuations [51]. Changes in ploidy and apomixis, although seldom taken into consideration, possibly help to explain the range expansion and diversification burst observed for Bignoniaceae and other Cerrado trees after the last glacial maximum [52] since apomicts are more flexible in terms of reproduction and at least cross-pollination independent [11,20]. This flexibility will certainly be important for the conservation of those trees in today’s scenario of anthropogenic pressure on the Cerrado threatened environment [53].
Our data showed that sporophytic apomictic populations of Cerrado trees have relatively high genetic diversity, in some cases even higher than sexual populations, and there were almost no individuals with identical ISSR profiles in apomictic populations. The higher within-populations variation found for both apomictic and sexual populations seems to be related to sexual reproduction events and possibly cross fertilization among individuals. Although there was a clearer difference among sexual and apomictic populations in H. ochraceus, one of the sexual populations was grouped with apomictic ones in all the analyses, which is evidence of relatedness among populations. Sporophytic facultative apomixis results both in reproductive assurance and maintenance of genetic diversity, which may have been vital for evolution and will be crucial for the conservation of Cerrado trees.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d17040254/s1, Figure S1: Photographs of agarose gels to three species (Eriotheca crenutlata, Eriotheca pubescens–Mao; Handroanthus ochraceus–UBC 898) used for analysis of presence and absence of bands. The white letter M represents the presence of molecular ladder (100pb) and the red arrows exemplify the patterns of bands chosen for the analysis. The blue arrows demonstrating the pattern of bands which were discarded for analysis for all individuals.Table S1: Primers, sequences, and optimum annealing temperature for each ISSR locus and each studied species.

Author Contributions

All authors helped in the study conception and design. R.C.M., C.M.-R., D.S.S. and M.G.M. collected the specimens. R.C.M. and M.G.M. did the laboratory experiments. R.C.M., D.S.S., C.M.-R., A.M.B., P.E.O. and E.L.B. wrote and corrected the text. The study was supervised by P.E.O. and D.S.S. All these authors approved this submission. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by the CAPES/Programa Nacional de Pós-Doutorado (PNPD 23038008068/2010-95) and by the Fundação de Amparo à Pesquisa do Estado de Minas Gerais—FAPEMIG (APQ 00593-11, APQ-02820-15 and RED0025316). We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes) for the Master’s scholarship to the first author and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Master’s scholarship to the second author, respectively.

Data Availability Statement

The original data underlying the conclusions of this article will be provided by the authors upon request, with the first author responsible for sharing the data.

Conflicts of Interest

The authors declare no competing interests.

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Figure 1. Distribution of sexual and apomictic populations of Eriotheca and Handroanthus in Southeast and Midwest Brazil. ECA = Eriotheca crenulata apomictic population; ECS = Eriotheca crenulata sexual population; EPA = Eriotheca pubescens apomictic population; EPS = Eriotheca pubescens sexual population; HOA = Handroanthus ochraceus apomictic populations; HOS = Handroanthus ochraceus sexual populations.
Figure 1. Distribution of sexual and apomictic populations of Eriotheca and Handroanthus in Southeast and Midwest Brazil. ECA = Eriotheca crenulata apomictic population; ECS = Eriotheca crenulata sexual population; EPA = Eriotheca pubescens apomictic population; EPS = Eriotheca pubescens sexual population; HOA = Handroanthus ochraceus apomictic populations; HOS = Handroanthus ochraceus sexual populations.
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Figure 2. Analyses of genetic distances and structure of the agamic complexes of Eriotheca crenulata and E. pubescens based on the genetic distance matrix for 74 individuals from 4 Eriotheca populations, using 111 ISSR loci. (A) A 3-D plot of principal coordinates analysis eigenvalues of the three main axes. The percentage of accumulated variance was Axis 1 = 64.36%, Axis 2 = 14.09% and Axis 3 = 12.13%. (B) Neighbor-joining dendrogram based on Nei genetic distance matrix. Bootstrap percentages were given above branches. (C,D) Bayesian analysis of genetic assignment. DK graphic above left. LnP graphic for 15 runs above right (mean ± standard deviation). (E–G). Graphical representations of genetic groups, where populations were separated by vertical bars. ECA = Eriotheca crenulata apomictic population; ECS = Eriotheca crenulata sexual population; EPA = Eriotheca pubescens apomictic population; EPS = Eriotheca pubescens sexual population.
Figure 2. Analyses of genetic distances and structure of the agamic complexes of Eriotheca crenulata and E. pubescens based on the genetic distance matrix for 74 individuals from 4 Eriotheca populations, using 111 ISSR loci. (A) A 3-D plot of principal coordinates analysis eigenvalues of the three main axes. The percentage of accumulated variance was Axis 1 = 64.36%, Axis 2 = 14.09% and Axis 3 = 12.13%. (B) Neighbor-joining dendrogram based on Nei genetic distance matrix. Bootstrap percentages were given above branches. (C,D) Bayesian analysis of genetic assignment. DK graphic above left. LnP graphic for 15 runs above right (mean ± standard deviation). (E–G). Graphical representations of genetic groups, where populations were separated by vertical bars. ECA = Eriotheca crenulata apomictic population; ECS = Eriotheca crenulata sexual population; EPA = Eriotheca pubescens apomictic population; EPS = Eriotheca pubescens sexual population.
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Figure 3. Analyses of genetic distances and structure of the agamic complex of Handroanthus ochraceus based on the genetic distance matrix for 117 individuals from six populations, using 104 ISSR loci. (A) 3-D plot of principal coordinates analysis eigenvalues of the three main axes. The percentage of accumulated variance was Axis 1 = 33.81%, Axis 2 = 19.35% and Axis 3 = 18.17%. (B) Neighbor-joining dendrogram based on Nei genetic distance matrix. Bootstrap percentages were given above branches. (C,D) Bayesian analysis of genetic of assignment. DK graphic above left. LnP graphic for 15 runs above right (mean ± standard deviation). (E) Graphical representation of genetic groups, where populations were separated by vertical bars. HOA = Handroanthus ochraceus apomictic populations; HOS = Handroanthus ochraceus sexual populations.
Figure 3. Analyses of genetic distances and structure of the agamic complex of Handroanthus ochraceus based on the genetic distance matrix for 117 individuals from six populations, using 104 ISSR loci. (A) 3-D plot of principal coordinates analysis eigenvalues of the three main axes. The percentage of accumulated variance was Axis 1 = 33.81%, Axis 2 = 19.35% and Axis 3 = 18.17%. (B) Neighbor-joining dendrogram based on Nei genetic distance matrix. Bootstrap percentages were given above branches. (C,D) Bayesian analysis of genetic of assignment. DK graphic above left. LnP graphic for 15 runs above right (mean ± standard deviation). (E) Graphical representation of genetic groups, where populations were separated by vertical bars. HOA = Handroanthus ochraceus apomictic populations; HOS = Handroanthus ochraceus sexual populations.
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Table 1. Species and populations studied and their embryonic pattern, ploidy level and chromosome number, and breeding system. Mono = monoembryonic; Poly = polyembryonic.
Table 1. Species and populations studied and their embryonic pattern, ploidy level and chromosome number, and breeding system. Mono = monoembryonic; Poly = polyembryonic.
Species
Municipality-State		CodeGeographical CoordinatesSample SizeEmbryonic PatternPloidy Level and Chromosome NumberBreeding SystemVoucher Number
E. crenulata (comb. n. E. gracilipes)
  Uberlândia-MGECS19°18′34″ S; 48°26′48″ W17Mono 3,42n = 2x = 92 1SexualHUFU-15008
  Caldas Novas-GOECA17°47′08″ S; 48°40′09″ W19Poly 42n = 6x = 276 1ApomiticHUFU-15122
E. pubescens
  Cristalina-GOEPS16°52′32″ S; 47°40′44″ W19Mono 3,42n = 4x = 184 1SexualHUFU-15073
  Catalão-GOEPA18°08′42″ S; 47°54′24″ W19Poly 3,42n = 6x = 276 1ApomiticHUFU-25854 *
H. ochraceus
  Uberlândia-MGHOS119°18′34″ S; 48°26′48″ W20Mono 22n = 2x = 40 2SexualHUFU-52585
  Pires do Rio-GOHOS217°11′37″ S; 47°45′03″ W20Mono 22n = 2x = 40 2SexualHUFU-55507
  Biribiri-MGHOS318°07′54″ S; 43°36′56″ W20Mono 52n = 2x = 40 5SexualHUFU-52678
  Córrego Danta-MGHOA119°41′12″ S; 46°02′20″ W19Poly 22n = 2x = 40; 2n = 4x = 80 2ApomiticHUFU-52593
  Fidalgo-MGHOA219°32′50″ S; 43°59′13″ W18Poly 52n = 4x = 80 5ApomiticBHCB-68100
  São José do Rio Preto-SPHOA320°47′10″ S; 49°21′32″ W20Poly 22n = 4x = 80 2ApomiticSJRP-29235
References: 1 = Marinho et al. 2014 [24]; 2 = Mendes et al. 2018 [20]; 3 = Mendes-Rodrigues et al. 2005 [17]; 4 = 11; 5 = Sampaio 2010 [27]; * Collection from a population very similar to the studied one. The original voucher was missing.
Table 2. Genetic diversity (GD) parameters. Percentage of polymorphic bands (P); Shannon index (I); expected heterozygosity (He) (± standard error); the number of loci in which pairs of individuals differ (NDL); and total loci analyzed in sexual and apomictic populations of Eriotheca crenulata, E. pubescens, and Handroanthus ochraceus. Similar letters after GD indexes indicate overlapping and non-significantly different values among populations of each genus.
Table 2. Genetic diversity (GD) parameters. Percentage of polymorphic bands (P); Shannon index (I); expected heterozygosity (He) (± standard error); the number of loci in which pairs of individuals differ (NDL); and total loci analyzed in sexual and apomictic populations of Eriotheca crenulata, E. pubescens, and Handroanthus ochraceus. Similar letters after GD indexes indicate overlapping and non-significantly different values among populations of each genus.
Populations (Breeding Systems)P (%)IHeNDLTotal Loci
Eriotheca crenulata
  ECS (sexual)50.510.294 ± 0.031 a0.201 ± 0.021 a3–25 loci93
  ECA (apomictic)59.600.363 ± 0.031 a0.251 ± 0.022 a2–27 loci88
  Species mean55.050.328 ± 0.0220.226 ± 0.015
Eriotheca pubescens
  EPS (sexual)66.250.396 ± 0.034 a0.273 ± 0.024 a6–25 loci71
  EPA (apomictic)68.750.396 ± 0.033 a0.271 ± 0.023 a0–26 loci73
  Species mean67.500.396 ± 0.0230.272 ± 0.017
Handroanthus ochraceus
  HOS1 (sexual)78.850.447 ± 0.267 a0.306 ± 0.193 a17–46 loci89
  HOS2 (sexual)74.040.355 ± 0.267 ab0.234 ± 0.190 ab14–44 loci101
  HOS3 (sexual)66.350.318 ± 0.268 b0.208 ± 0.187 b13–41 loci87
Sexual populations mean73.080.373 ± 0.0660.249 ± 0.051
  HOA1 (apomictic)53.850.316 ± 0.307 b0.217 ± 0.215 b10–34 loci82
  HOA2 (apomictic)72.120.342 ± 0.250 b0.221 ± 0.174 b14–42 loci87
  HOA3 (apomictic)52.880.267 ± 0.280 b0.177 ± 0.194 b12–37 loci88
  Apomictic populations mean59.620.308 ± 0.0380.205 ± 0.024
  Species mean66.350.341 ± 0.0600.227 ± 0.043
Table 3. Analysis of molecular variance (AMOVA) in sexual and apomictic populations of Eriotheca crenulata, E. pubescens and Handroanthus ochraceus.
Table 3. Analysis of molecular variance (AMOVA) in sexual and apomictic populations of Eriotheca crenulata, E. pubescens and Handroanthus ochraceus.
SpeciesSource of VariationDegrees of FreedomSum of SquaresVariance ComponentsTotal Variance Percentagep-Value
E. crenulata
Among populations1172.6769.23253%<0.001
Within populations34238.4457.01347%<0.001
Total35411.12116.245100%<0.001
E. pubescens
Among populations1169.4798.41847%<0.001
Within populations36343.1279.53153%<0.001
Total37512.60517.950100%<0.001
H. ochraceusAmong populations5875.1388.32239.00<0.001
Within populations111420.76612.80061.00<0.001
Grouped by breeding system
Among groups/breeding system1183.9140.1991.00<0.046
Among populations4688.7608.16838.00<0.001
Within populations1111441.10412.98361.00<0.001
Grouped by Bayesian analysis
Among groups (HOS1, HOA1, HOA2, HOA3 and HOS1, HOS2)1290.046290.04612.00<0.001
Among populations4582.777145.69430.00<0.001
Within populations1111440.95412.98258.00<0.001
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Marinho, R.C.; Mendes, M.G.; Mendes-Rodrigues, C.; Bonetti, A.M.; Borba, E.L.; Oliveira, P.E.; Sampaio, D.S. Genetic Diversity in Sporophytic Apomictic Neotropical Savanna Trees: Insights from Eriotheca and Handroanthus Agamic Complexes. Diversity 2025, 17, 254. https://doi.org/10.3390/d17040254

AMA Style

Marinho RC, Mendes MG, Mendes-Rodrigues C, Bonetti AM, Borba EL, Oliveira PE, Sampaio DS. Genetic Diversity in Sporophytic Apomictic Neotropical Savanna Trees: Insights from Eriotheca and Handroanthus Agamic Complexes. Diversity. 2025; 17(4):254. https://doi.org/10.3390/d17040254

Chicago/Turabian Style

Marinho, Rafaela Cabral, Mariana Gonçalves Mendes, Clesnan Mendes-Rodrigues, Ana Maria Bonetti, Eduardo Leite Borba, Paulo Eugênio Oliveira, and Diana Salles Sampaio. 2025. "Genetic Diversity in Sporophytic Apomictic Neotropical Savanna Trees: Insights from Eriotheca and Handroanthus Agamic Complexes" Diversity 17, no. 4: 254. https://doi.org/10.3390/d17040254

APA Style

Marinho, R. C., Mendes, M. G., Mendes-Rodrigues, C., Bonetti, A. M., Borba, E. L., Oliveira, P. E., & Sampaio, D. S. (2025). Genetic Diversity in Sporophytic Apomictic Neotropical Savanna Trees: Insights from Eriotheca and Handroanthus Agamic Complexes. Diversity, 17(4), 254. https://doi.org/10.3390/d17040254

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