Evolution of Ceratozamia cycads: A proximate-ultimate approach Medina-Villarreal, Anwar; González-Astorga, Jorge; Espinosa de los Monteros, Alejandro
Molecular phylogenetics and evolution,
October 2019, 2019-10-00, 20191001, Volume:
139
Journal Article
Peer reviewed
A. Typical specimen of a plant of the genus Ceratozamia. B. Ontogenetic transformation by estimating the difference in the value of the leaflets shape index between seedlings and adults. C. Phylogeny ...of Ceratozamia species. In each terminal typical leaflets of each species are presented.
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•Comprehensive phenotypic assessment of populations-species of a cycad genus.•Molecular phylogeny supports two clades: ‘miqueliana’ and ‘mexicana’.•Ceratozamia was originated at the S of Mexico and diversified in the last 3 Mya.•Empirical evidence of punctuated evolution in the lineages encompassed by Ceratozamia.•Ontogeny also traces the evolutionary history of the Ceratozamia species.
Evidence suggests that past climatic fluctuations affected speciation of extant cycads. However, empirical genetic and morphological evidence explaining patterns and processes of species diversification are scarce. There are some explanations for the origin and evolution of the genus Ceratozamia, but with inconclusive results. To elucidate the evolution of Ceratozamia, we used genetic and phenotypic sources as empirical data, which were applied in a ‘proximate-ultimate’ framework (ecological and evolutionary scale, respectively). Our results suggested that the evolutionary mechanisms of speciation were shaped by deterministic (natural selection-adaptation) driven by climatic conditions associated to water stress, and probably enhanced by stochastic processes (gene drift and inbreeding). In general terms, punctuated evolution models were those that best explained the patterns of speciation throughout the phylogenetic history of the lineages encompassed in the genus Ceratozamia. Finally, we provide empirical evidence on the tempo and mode of the evolution of a ‘living plant fossil’.
The Cycadales contain 11 nonproblematic genera and approximately 331 species where, in a number of cases, delimitation and circumscription is not so clear. Ceratozamia, the most diverse cycad genus ...in Mexico, clearly illustrates this situation because a large percentage (close to 70%) of the 28 currently valid species in the genus was recently described on the basis of inconspicuous differences. We evaluated population‐level morphological variation (i.e. phenotype) in related plants of Ceratozamia that share geological and ecological units, seeking a refined taxonomic assessment of their populations in an explicitly evolutionary context. The populations/species of interest included the type species Ceratozamia mexicana, as well as the taxa Ceratozamia brevifrons, Ceratozamia decumbens, and Ceratozamia morettii. Data analysis was performed using uni‐ and multivariate techniques on morphological variability, which showed statistically significant differences. The characters ‘leaflet width’ and ‘leaflet shape’ supported diagnostic distinctions between groups of populations, and implied a classificatory rearrangement with nomenclatural consequences. This research is an initial step in the detailed, statistics‐oriented study of phenotypic variation in the Ceratozamia populations of central Veracruz in Mexico that will allow the construction of evolutionary hypotheses in the context of phylogeography and historical demography.
Abstract
We analysed the genetic divergence and morphology of the aedeagus (i.e. phallobase and parameres) in Canthon cyanellus at different geographical levels. The results from both approaches were ...compared with the current taxonomic assignment of the C. cyanellus complex, which includes three subspecies. We found a high variation in all the morphological characters of the aedeagus in the populations analysed; the morphometric variation was not geographically structured, either by population or by region. The genealogical analysis indicates a significant genetic structure that does not match either the morphological variation in the male genitalia or the previous subspecific taxonomic classification. Our results suggest that the morphological variation of the aedeagus is seemingly not an isolating reproductive barrier and that the intra- and interpopulation morphological variability of the aedeagus in the C. cyanellus complex does not permit the division into several species. We suggest that other evolutionary forces, such as genetic drift and sexual selection, have influenced the evolution of the male genitalia and the incipient differentiation of this species complex.
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•Phylogeographic analyses of Canthon cyanellus in Mexico reveals lineages historical differentiation.•The divergence of this Neotropical group occurred during the ...Pleistocene.•Geological events and glacial cycles influenced the geographic structure of the lineages.•The demographic history suggests post-glacial expansions.•Not all the current valid subspecies are supported by the molecular analysis.
Canthon cyanellus is a roller dung beetle with a wide distribution range in the tropical forests of the New World. In Mexico, it inhabits the Pacific and the Gulf coasts, the Yucatan Peninsula and the south mainly in the State of Chiapas. This species shows a wide geographical variation in cuticle color, which has been used as defining trait for subspecies. In this study we analyzed the phylogeographic and demographic history of the Mexican populations of C. cyanellus using DNA sequences of the nuclear ITS2, and the mitochondrial COI and 16S genes. We found that not all the current valid subspecies are supported by the molecular analysis. The populations are genetically and geographically structured in five lineages. The diversification events that gave origin to the main lineages within this species complex occurred during the Pleistocine in a time range of 1.63–0.91Myr. The demographic history of these lineages suggests post-glacial expansions toward the middle and the end of the Pleistocene. The combined data of mitochondrial and nuclear DNA suggest that the phylogeographic structure and demographic history of the C. cyanellus populations are the result of: the geological and volcanic activity that occurred from the end of the Pliocene to the Pleistocene; and the contraction and expansion of tropical forests due to the glacial and inter-glacial cycles during the Pleistocene. Landscape changes derived from historical events have affected the demographic history of the populations of this species. The results presented here point to the need to review the taxonomic status and delimitation of the lineages encompassed in the Canthon cyanellus complex.
Plant invasions have a huge impact on the health of ecosystems and human well-being. The invasion risk varies with the introduction pathway, the propagule pressure, and the genetic diversity of the ...founding population. We performed a systematic review and meta-analysis of 30 studies reporting the genetic diversity of 31 plant species in their invasive and native ranges. We evaluated if patterns of genetic diversity differ between ranges and whether these responses are influenced by life-history traits, hybridization, polyploidization, and habitat condition. We found that invasive populations had significantly lower genetic diversity and higher inbreeding than native populations. In fragmented and degraded habitats, the genetic diversity of invaders was lower, but inbreeding was not affected. Polyploid invaders with hybrid capacity also showed lower genetic diversity. Invasive herbs with vegetative propagation were more sensitive to the loss of genetic diversity and had higher levels of inbreeding. Our synthesis showed that the genetic response in the invaded range could result from historical processes, such as founder and bottleneck events. Traits such as selfing are more likely to preserve the signatures of founder events and influence the genetic diversity in invasive populations. Additionally, clonality seems to be the predominant reproduction system in the invaded range.
Ecological and microevolutionary perspectives were used to investigate signs of background extinction in two endemic species. We studied relict populations of the cycad Dioon caputoi, contrasting its ...population structure and neighborhood size with those of Dioon planifolium as a demographically healthier reference population. Population dynamics analysis was performed on two populations of D. caputoi through Integral Projection Models and genetic neighborhoods compared between species through 172 Inter Simple Sequence Repeat loci performed in one population of each of the two study species. The D. caputoi populations mostly comprised adult plants, while D. planifolium presented mainly juvenile individuals. Dioon caputoi showed equilibrium in population growth (i.e., λ ≈ 1), with low recruitment, and its genetic neighborhood revealed highly related individuals in a unique distance class (rij = 0.407, 33 m). A contrasting pattern was found in D. planifolium, which showed higher relatedness in the first distance class (rij = 0.543, 5 m), gradually decreasing to 20 m. The discrepancies between the two species reflect different strategies of persistence. Dioon caputoi conserves a relict dynamics with signs of a multigenerational, attritional loss of reproductive fitness, while D. planifolium does not. This study furthers our understanding of the background extinction process and the information will thus contribute to the management and conservation of this endangered species.
1. Ecological and microevolutionary perspectives were used to investigate signs of background extinction in two mexican endemic species of cycads (Dioon caputoi and D. planifolium).
2. D. caputoi conserves a relict dynamics with signs of a multigenerational, attritional loss of reproductive fitness, while D. planifolium does not.
To understand the evolutionary history of species, it is necessary to know the mechanisms for reproductive isolation, divergence-time between populations, and the relative action of the evolutionary ...forces (e.g., mutation, genetic drift, gene flow) within and between populations of the same, or closely related species. Although
Canthon
is one of the more diverse genera of neotropical beetles, insufficient research has been done to comprehend the divergent patterns that explain its speciation process. The absence of diagnostic morphological characters and the wide geographic variation of qualitative traits in Scarabaeinae obscures species delimitation, genealogical limits between populations, and its taxonomy.
Canthon cyanellus
is one of the best-known species in ecological and evolutionary aspects. It is a widely distributed species in the tropical forests of America. Also, the current deforestation has facilitated its incursion into open areas. Individuals from different populations have similar morphological characters but show wide variation in body color throughout their distribution, which makes it difficult to delimit the subspecies that comprise it. Recently, studies have been carried out to elucidate the pre-and postzygotic isolation mechanisms between populations and the historical biogeographical processes favoring cladogenesis events during the Pleistocene. Morphological variation of the male genitalia does not correspond to the phylogeographic structure. However, the morphological differences in one of the pieces of the endophallic sclerites have allowed a preliminary delimitation of some genetically differentiated clades. Finally, we consider that the joint analysis of traditional morphological taxonomy and phylogeography is important to understand the speciation process in the
C. cyanellus
complex.
•Leaflet anatomy for the C. miqueliana complex described for the first time.•The confusion of C. becerrae with C. zoquorum has been solved.•Leaflet anatomy conforms C. becerrae as a good ...species.•Plant anatomy has proved useful for solving conflicting molecular data.
The Ceratozamia miqueliana species complex consists of six closely related species that exhibit similar gross morphology, but a wide range of leaflet shape from widely obovate in C. euryphyllidia and C. hondurensis to oblanceolate in C. zoquorum. However, despite the clear leaflet size variation, the taxon delimitation within the complex has been suggested to be uncertain when considering other traits, giving rise to doubts about the taxonomic validity of taxa, particularly of C. becerrae. Previous studies have shown that anatomical traits might be effective diagnostic characters to delimitate closely related cycad species. This study reviewed the anatomical variation of the Ceratozamia miqueliana species complex. We provide taxonomic treatment in the basis of anatomical trait variation. Although the six species occupy relatively mesic environments in tropical rainforest habitats, we found that some species exhibited leaflet anatomical traits associated to water stressed environments, suggesting historical adaptation to xeric conditions. The anatomical trait variation presented in this study agrees with a recent molecular phylogenetic study, clears up doubts on species relationships in the C. miqueliana complex, and validates the taxonomic recognition of C. becerrae.
• Background and Aims Genetic structure and variability were examined in the only three extant populations of the narrow‐endemic tree Antirhea aromatica (Rubiaceae, Guettardeae), an endangered ...species of the tropical forest of eastern Mexico. Patterns of genetic diversity within and among populations for adult plants and seedlings were obtained. • Methods Allozyme electrophoresis of 15 loci was conducted and the data analysed with statistical approximation for obtaining genetic diversity, structure and gene flow. • Key Results The mean expected heterozygosity (He) in the adult and seedling populations was 0·18 ± 0·08 and 0·20 ± 0·09, respectively. The genetic variation explained by differences among populations was 51 and 35 %, for adult and seedling populations, respectively. On average, gene flow between paired adult populations was low (Nm = 0·26 ± 0·09), compared with other trees from the tropical forest. • Conclusions The results indicated that the populations evaluated have high genetic variability, compared with other endemic and geographically narrowly distributed plant species, in areas with high levels of environmental heterogeneity (e.g. tropical forests). The conservation implications of the results are discussed, and in this regard it is proposed that A. aromatica should be considered as an indicator species with economic potential. It is suggested that sustainable management practices should be implemented and that the areas where the species is distributed should be declared a natural reserve to ensure the species conservation.
The study of morphological variation in heterogeneous environments provides evidence for understanding processes that determine the differences between species and interspecific adaptive strategies. ...In 14 populations of two closely related cycads from the genus Zamia (Zamia loddigesii and Z. prasina), the phenotypic variation was analyzed based on 17 morphological traits, and this variability was correlated with environmental conditions across the populations. Despite the significant inter-population variation observed in the two species, greater inter-specific differences were observed based on generalized linear models. Individuals of all populations except for the Macuspana (Tabasco) population of Z. prasina were separated into two discrete groups in a multivariate space (non-metric multidimensional scaling). Macuspana plants overlapped marginally with the multivariate space defined by plants in the four Z. loddigesii populations. Remarkably, Macuspana is geographically located at the distribution limits of both species that occur in close proximity expressing traits that resemble either of the two species. The heterogeneous environment seems to play a determining role in the phenotypic expression of both species. The variation found could be related to the local ecological adaptions that tend to maximize the populations adaptation.
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