Research Article Quaternary origin and genetic divergence of the endemic cactus Mammillaria pectinifera in a changing landscape in the Tehuacán Valley, Mexico

Abstract

ABSTRACT. The endemic Mexican cactus, Mammillaria pectinifera, shows low dispersal capabilities and isolated populations within the highly dissected landscape of Tehuacán Valley. These characteristics can restrict gene flow and act upon the genetic divergence and speciation in arid plants. We conducted a phylogeographic study to determine if the origin, current distribution, and genetic structure of M. pectinifera were driven by Quaternary geomorphic processes. Sequences of the plastids psbA-trnH and trnT-trnL obtained from 66 individuals from seven populations were used to estimate genetic diversity. Population differentiation was assessed by an analysis of molecular variance. We applied a stepwise phylogenetic calibration test to determine whether species origin and genetic divergence among haplotypes were temporally concordant with recognizable episodes of geomorphic evolution. The combination of plastid markers yielded six haplotypes, with high levels of haplotype diversity (h = 0.622) and low nucleotide diversity (π = 0.00085). The populations were found to be genetically structured (F ST = 0.682; P < 0.00001), indicating that geographic isolation and limited dispersal were the primary causes of genetic population differentiation. The estimated origin and divergence time among haplotypes were 0.017-2.39 and 0.019-1.237 mya, respectively, which correlates with Pleistocene tectonics and erosion events, supporting a hypothesis of geomorphically-driven geographical isolation. Based on a Bayesian skyline plot, these populations showed long term demographic stability, indicating that persistence in confined habitats has been the main response of this species to landscape changes. We conclude that the origin and haplotype divergence of M. pectinifera were a response to local Quaternary geomorphic evolution.

Evaluating the monophyly of Mammillaria series Supertextae (Cactaceae)

“…Supertextae, four clades are formed, two of which have distinctive climatic and topographic characteristics: Clade S1 (M. haageana, M. albialanta, M. dixanthocentron and M. supertexta), with species that are distributed in warm zones mainly at altitudes ranging from 447 to 2318 meters in thorn and tropical deciduous forests; and Clade S2 (M. haageana, M. albilanata and M. flavicentra), with species that are distributed in temperate zones at altitudes that range mainly from 1285 to 2518 meters in pine-oak forests. The environmental, geological and topographic differences between closely related species produced during climatic changes suggest differential selection pressures and local adaptation, which could have driven the speciation process (Mastretta-Yanes et al 2015;Aquino et al 2021), as has been suggested for Mammillaria pectinifera (Cornejo-Romero et al 2014), Cephalocereus columna-trajani (Cornejo-Romero et al 2017) and the genus Epithelantha (Aquino et al 2021). Mammillaria haageana and M. albilanata represent a complex that extends widely in southern Mexico.…”

“…The Mammilloid clade originated approximately 8.62 Mya (95% HPD = 5. 83-12.56;Hernández-Hernández et al 2014), and within Mammillaria, it is likely that M. ser. Supertextae is a recently divergent group that originated in the Neogene-Quaternary transition approximately 2.1 Mya (95% HPD = 0.91-3.47).…”

“…To evaluate the monophyly of the subgenera and series recognized by Hunt et al (2006) To estimate divergence times, we used the credibility interval around the estimated age of the Mammilloid clade (5. 83-12.56 Mya;Hernández-Hernández et al 2014). We inferred a time-calibrated phylogenetic tree using a BI approach implemented in BEAST (v. 2.6.1, Bouckaert et al 2019).…”

“…We chose two chloroplast markers, the rpl16 intron and the intergenic spacer psbA-trnH. In Cactaceae, both markers have been used to resolve phylogenetic relationships (Korotkova et al 2010;Cruz et al 2016;Barrios et al 2020), including Mammillaria (Butterworth and Wallace 2004;Vázquez-Sánchez et al 2013;Hernández-Hernández et al 2014); therefore, there are many sequences available in GenBank that can be used to expand the sampling of terminals, including sister groups and outgroups essential for testing the monophyly (Korotkova et al 2017) of M. ser. Supertextae.…”

Landscape genetics reveals inbreeding and genetic bottlenecks in the extremely rare short-globose cacti Mammillaria pectinifera (Cactaceae) as a result of habitat fragmentation

“…Most of the previous population genetic studies within the Cactaceae family have been mainly conducted on columnar and short globose cacti using allozymes ( Nassar et al., 2001 , Hamrick et al., 2002 , Moraes et al., 2005 , Parra et al., 2008 ), RAPDs ( Clark-Tapia et al., 2005 ) and microsatellites ( Figueredo et al., 2010 , Castro-Felix et al., 2013 , Solórzano et al., 2014 ). Cornejo-Romero et al. (2014) found that populations of species of Mammillaria were genetically structured indicating that geographic isolation and limited dispersal were the primary causes of genetic population differentiation.…”