https://orcid.org/0000-0002-4691-1091
Figures
Abstract
Cacti have undergone some of the fastest diversification events in the plant kingdom despite their slow growth rates and extended generation times. This rapid evolution may be driven by intense ecological interactions. Here we tested, for the first time, the evolutionary dynamics of the ecological niches of Gymnocalycium species focusing on two key environmental factors: temperature and precipitation. To explore patterns of niche conservatism and/or evolution and identify major contributing factors, we reconstructed ancestral niches associated with these climatic dimensions using the binned ancestral range coding method. Our findings reveal that (1) the climatic-niches of narrow-ranged Gymnocalycium species are not highly conserved across the phylogeny (i.e., niches are evolving), (2) the evolutionary dynamics of thermal and precipitation niches across the Gymnocalycium phylogeny do not follow similar patterns, (3) a bioregion-specific pattern of niche evolution exists, and (4) the Early–Middle Pleistocene glaciations (i.e., GPG and three Post-GPG phases) potentially drove the patterns of lineage divergence in Gymnocalycium species, triggering the evolution of climatic niches. These results suggest that (i) Gymnocalycium species with fascicular roots may require special attention for conservation, (ii) in a warming climate, the species distributed in the South American transition zone, South Brazilian dominion, and Chacoan dominion may face serious risks, and (iii) the relatively ‘more tight-less tight’ pattern in conserving the precipitation and temperature niches could be a strategy for conserving the critical variable at the expense of the other. This study has not only provided valid insights into the evolutionary history of Gymnocalycium species but also highlights the importance of conservation efforts, essential to protect these species.
Citation: Nair RR, Sérsic AN, Demaio PH, Perotti SB, Gurvich DE (2025) ‘More tight-less tight’ Patterns in the Climatic Niche Evolution of Gymnocalycium (Cactaceae): Were Pleistocene Glaciations a Prelude? PLoS One 20(5): e0323758. https://doi.org/10.1371/journal.pone.0323758
Editor: Patrick R. Stephens, Oklahoma State University, UNITED STATES OF AMERICA
Received: December 9, 2024; Accepted: April 14, 2025; Published: May 20, 2025
Copyright: © 2025 Nair et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: The financial support received from the British Cactus and Succulent Society (BCSS, UK) for the project titled “Evolutionary history of four Gymnocalycium species of the Sierras Pampeanas at intra- and interspecific level” helped in part to complete this study. Details of the project can be found at: https://bcss.org.uk/evolutionary-history-of-four-gymnocalycium-species-of-the-sierras-pampeanas-at-intra-and-interspecific-level/. In addition, this research received financial support from FONCyT (PICT 2016-0077) and SECyT-FCEFyN-UNC (Universidad Nacional de Córdoba, Argentina). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
In evolutionary studies, a strong link between environmental conditions and speciation in Cactaceae has been established, with environmental factors exerting selective pressures on floral traits [1], maintaining species boundaries [2], and influencing lineage diversification [3,4]. The concept of species’ niches is central in understanding the patterns and boundaries of species’ response to the environment [5,6]. Species’ fundamental niche—the full suite of abiotic conditions supporting its existence without biotic interactions—evolves over time [7–10]. Recent studies have highlighted the evolutionary dynamics of fundamental niches in diverging lineages, enriching our understanding of biogeographic patterns and evolutionary histories [8,9,11–16]. Despite the possible influence of environmental selective pressures on the evolution of different cactus life-forms [17], their natural geographic distribution is also largely, but differentially, shaped by various environmental gradients [18]. For instance, low-temperature sensitivity influences the distribution of columnar cacti [17,19,20], high-temperature [21,22] and the variability of summer rainfall [17] control the distribution of globose cacti, summer rainfall trends affect opuntioid cacti [17], high-moisture conditions support epiphytic cacti distribution [23], and seasonal rainfall patterns influence pereskioid cacti [24]. Given the role of environmental gradients in cactus diversification, linking phylogeny and environment offers new perspectives on niche evolution, indicating whether niches are conserved or divergent across phylogenies [9,15]. Contrary to the common perception that cactus species may withstand future climatic fluctuations, as they are heat and drought tolerant, a recent study [25] indicates that climate change could be the primary risk factor, causing the extinction of many cactus species. Hence, understanding the tendency of cactus species to retain their environmental niches across the phylogeny may help the researchers to better predict their ability to cope with changing climates (i.e., adaptation to novel environmental conditions) [13,26,27].
To the best of our knowledge, a detailed study on the evolutionary dynamics of climatic niches, taking ancestral niches into account and including a dated phylogeny, has never been attempted in any genus of the family Cactaceae. In this study, we focus on the genus Gymnocalycium Pfeiff. ex Mittler (Cactaceae), a group of globose cacti species, native to southern South America, that includes around 50 species [28–30]. The currently known distribution of Gymnocalycium species in South America spans a broad range, extending from 16.70oS to 45.19oS, and from 53.10oW to 69.30oW, covering five countries: Argentina, Bolivia, Paraguay, Uruguay, and Brazil. It is one of the most important plant genera of the Cactaceae family, as it is species-rich, and is developing a growing interest among both professional and amateur collectors, of succulent or ornamental plants [28,31]. This genus is of particular interest for studying environmental niche evolution across phylogeny due to its (1) high level of endemism [29,31,32], (2) adaptation to heterogenous environmental conditions [29,33–36], and (3) presence at different ecological regions across a range of altitudinal gradients [21,29–32,37,38].
In this study, we tested the evolutionary dynamics of climatic niches across the Gymnocalycium phylogeny, asking the following questions.
- 1. Are the climatic-niches of narrow-ranged Gymnocalycium species highly conserved across the phylogeny, indicating niche conservatism?
Various well-established hypotheses, such as niche breadth-range size [39,40], range size-niche breadth [41–43], and range shift-niche breadth [44], that connect niche breadth with the size of geographic ranges, suggest a positive association between niche breadth and geographic range size [45–49]. In a phylogenetic framework, studies on climatic-niche evolution linked with range size suggest that the rate of niche evolution in narrow-ranged species may be lower (i.e., more conserved), compared to wide-ranged species [11,50–52]. However, inter-specific variations in the utilization of environmental space from the total environmental space of the clade may result in the divergence of niches [50]. There are inter-specific differences in the utilization of environmental conditions by the Gymnocalycium species. Hence, we expect that the climatic-niches of narrow-ranged Gymnocalycium species may not be highly conserved across the phylogeny.
- 2. Do the evolutionary dynamics of thermal and precipitation niches across the Gymnocalycium phylogeny follow similar patterns?
As there are strong selective pressures of temperature and precipitation variables on Gymnocalycium species distribution [29,30,33,37,38,53], we expect that the evolutionary dynamics of thermal and precipitation niches across the Gymnocalycium phylogeny do not follow similar patterns.
- 3. Does a bioregion-specific pattern of niche evolution exist with respect to temperature and precipitation dimensions?
Temperature and precipitation variables are central in biogeographic regionalization [54], and the Neotropics have diverse biogeographic regions (bioregions) [55,56]. Hence, we expect a bioregion-specific pattern of niche evolution in Gymnocalycium.
- 4. Did the Early–Middle Pleistocene glaciations (i.e., GPG and three Post-GPG phases) potentially drive the patterns of lineage divergence in Gymnocalycium species, resulting in the evolution of temperature and precipitation niches?
Several studies have linked the evolution of climatic niches with lineage divergence events [14,16,57–61]. In South America, the Great Patagonian Glaciation (GPG; 1.0–1.1 Mya) followed by three Middle Pleistocene glaciations (Post-GPG 1, 2 & 3) [62,63] greatly influenced species diversifications and distributions [64–67], as the glacial cycles of advancement and retreat had significant effects on the climate in southern South America (the regions south of 15oS)[68]. Hence, we expect that the Early–Middle Pleistocene glaciations (i.e., GPG and three Post-GPG phases) played a significant role in lineage divergence in Gymnocalycium species, leading to the evolution of temperature and precipitation niches.
Materials and methods
Study species and data collection
For the present study, we used 40 Gymnocalycium species (S1 Table) that were included in the best inter-specific phylogenetic hypothesis of the Gymnocalycium group [69] available to us. The occurrence data of these species were extracted from a variety of sources: field surveys conducted by the authors (RRN, ANS, PHD, SBP, and DEG), online databases such as Global Biodiversity Information Facility (www.gbif.org) [70], iNaturalist (www.inaturalist.org), cactus and succulent field number (www.cl-cactus.com), ecoregistros (www.ecoregistros.org), cactus habitat (www.cactushabitat.com), cactus in habitat (www.cactusinhabitat.org), personal communication (Roberto Kiesling), herbarium collection (CTES herbarium; Instituto de Botánica del Nordeste, Argentina), Documenta Florae Australis (www.darwin.edu.ar/iris), and published literature [71–73]. Documented occurrences with no precise geographic coordinates but with exact locality information were extrapolated using the Google Earth software to find corresponding geo-coordinates. Each occurrence locality was visually inspected for accuracy using a geographic information system platform (QGIS version 3.36) [74], and questionable records were removed from the dataset. A spatial thinning procedure with a distance threshold of 5.2 km was performed on the dataset to keep only one presence point per pixel in the environmental raster layers (see below for more details). The thinning procedure was executed using the spThin R package [75]. The total number of records in the final dataset was 448 (Fig 1); species-wise, a maximum of 54 records for G. pflanzii and a minimum of 2 records for G. chacoense were present in the dataset.
The distribution of forty species of Gymnocalycium included in the present study across five South American countries: Argentina, Brazil, Bolivia, Paraguay, and Uruguay. The shapefiles of countries were sourced from DIVA-GIS (https://diva-gis.org), a free and open-source geographic information system.
The bioclimatic raster layers (2.5 arcmin resolution; 19 variables) that serve as the reference of current climate (1979–2013) were downloaded from the PaleoClim database [76], that hosts the upscaled version of high-resolution CHELSA environmental layers [77]. From the climatic dataset, we removed four interactive variables that combine both precipitation and temperature measurements (bio8: mean temperature of wettest quarter, bio9: mean temperature of driest quarter, bio18: precipitation of warmest quarter, and bio19: precipitation of coldest quarter), as these variables are known to possess spatial anomalies [78–82].
Accessible area hypothesis
Defining the parts of the world that are accessible to species via dispersal over relevant periods of time (area M) [7,83], with which species’ response to environment can be estimated [84], is a crucial component in the characterization of ancestral environmental niches [9]. If niche estimates of a species are derived from the presence data alone (i.e., only from the occupied ranges), it may inflate the estimates of niche change over time which lead to erroneous reconstruction of ancestral niches, as characterization of niches solely based on realized niche is incomplete [8,9]. Incorporating the accessible areas to quantify the utilization of environmental conditions helps to identify cases in which niches estimates are likely to be uncertain [9]. Under the current climate scenarios, the estimation of area M was performed using a simulation-based approach [84]; a process that critically considers dispersal parameters (i.e., dispersal kernel and number of dispersal events) and current distributional knowledge [84,85] for each of the Gymnocalycium species. The M simulation procedure was performed using the grinnell R package (version 0.0.22; https://github.com/fmachados/grinnell.git) [84]. We used a log-normal dispersal kernel for the M simulations, as it is best suited for seed dispersal studies [86–89]. Total number of dispersal events was set to 35 (~one dispersal event/year for 35 years, covering the time range of climate data), with two as a maximum number of dispersers that move from each pixel per dispersal event. The parameter (maximum number of dispersers) splits the suitability range (0–1) of a colonized cell into a number of intervals equal to the value of the parameter [84]. In this case, the suitability range (0–1) is divided into two equal intervals: 0.0–0.5 and 0.5–1.0. In each dispersal event, two dispersers will move from a colonized cell if the suitability of that cell exceeds 0.5, and only one disperser will move if the suitability is less than or equal to 0.5. Three different values (0.25, 0.50, and 0.75) were screened for kernel standard deviation (SD) that indicates the spread of dispersal kernel. Parameterization of the M simulations is detailed in the supporting information (S2 Table). Finally, the Ms that were simulated with an SD of 0.50 were chosen for further analyses (Fig 2). This selection was performed by superimposing all M polygons on the South American map, and choosing the appropriate Ms based on visual inspection and expert knowledge. It was not possible to simulate Ms for eight species due to a low number of records (G. chacoense, G. glaucum, G. horstii, G. kieslingii, G. oenanthemum, G. robustum, G. stenopleurum, and G. uebelmannianum, and for those species, environmental information was sourced from the occurrence points only.
Simulated accessible areas of Gymnocalycium species used in this study. The M simulations were not successful for eight species: G. chacoense, G. glaucum, G. horstii, G. kieslingii, G. oenanthemum, G. robustum, G. stenopleurum, and G. uebelmannianum. The red dots represent the known occurrences. The shapefiles of countries were sourced from DIVA-GIS (https://diva-gis.org), a free and open-source geographic information system.
Phylogenetic hypothesis and dating
For molecular dating, we performed a Bayesian phylogenetic reconstruction using the aligned DNA sequence matrix (6195-bp) of four plastid markers viz., atpI-atpH, petL-psbE, trnT-trnL-trnF, and trnK-matK, that was employed earlier for developing the latest available phylogeny of the Gymnocalycium group that display inter-specific relationships [69]. The ingroup taxa comprised 40 species of Gymnocalycium. Matucana polzii, Oreocereus celsianus, Uebelmannia pectinifera, and Stetsonia coryne were used as outgroup taxa, following Demaio et al. [69]. The appropriate nucleotide substitution model was identified as GTR + G based on the lowest Akaike information criterion (AIC), using the jModelTest software [90]. To quantify the molecular substitution rates for estimating divergence times, we used an uncorrelated relaxed clock [91] with a log-normal relaxed distribution in combination with Yule tree priors [92]. The time to most recent common ancestor (tMRCA) for the Trichocereeae clade comprising Gymnocalycium species, M. polzii, and O. celsianus was set to 6.12 Mya, following Hernández-Hernández et al. [93]. A root height of 6.57 Mya was set as the divergence time estimate between the Trichocereeae group and the clade comprising U. pectinifera and S. coryne. We set the length of MCMC chain to 5 X 107 generations, with parameter values sampled every 5000 generations. The input file was prepared in BEAUti, and the divergence time estimation was performed using BEAST v.1.7.5 [94]. The MCMC output was checked for the convergence of estimated parameters in Tracer v.1.7 [95], and the first 10% of the trees were removed as burn-in [96]. A maximum clade credibility (MCC) tree was constructed by combining the sample trees using TreeAnnotator v.1.10.4 [97], discarding 5000 sampled states. The final tree was visualized in FigTree v.1.4.4 [98].
Characterization of ancestral niches
As our primary interest was to study the ancestral niche characteristics related to temperature and precipitation dimensions, we used two environmental layers that correspond to mean annual temperature (bio1; hereafter temperature) and annual precipitation (bio12; hereafter precipitation) for further analyses. We selected bio1 and bio12, as these variables reflect the most important aspects of the overall climatic distribution of a species [58,99]. A Binned Ancestral Range (BAR) reconstruction procedure [8,9] that explicitly takes the incomplete characterization of niches (i.e., niche truncation) [8] into consideration was employed independently for these two variables [9,14,16]. Recent years have witnessed a growing interest in using this approach to reconstruct the ancestral niches [9,14,16,100]. Summary statistics of these two variables (i.e., mean, standard deviation, median, minimum and maximum values, and quartiles) based on the accessible areas (Ms) and the occurrence localities, were estimated separately. This estimation of the full niche ranges was performed within the union of all Ms [9] of Gymnocalycium species. Then, we parsed the full niche ranges into equal-sized discrete bins (S3 Table) separately for temperature (~1oC width) and for precipitation (~100 mm width). The BR (binned-range) character coding strategy embedded in the BAR method is as follows [9]: (1) All occurrences, and the bins that lie between minimum and maximum values of occurrence points within the area M are marked as “present” (code - 1), (2) If there are unoccupied conditions within the M beyond the limits of occupied conditions, as estimated in the previous step, such bins are marked as “absent” (code - 0), and (3) If the environmental limits at either end of the occurrence information overlap with the boundary conditions of M, the environmental bins beyond these limits are marked as “uncertain” (code -?). In the binning scheme of species for which the M simulation failed due to a low number of records, the bins located beyond the lower and upper limits of the occupied environmental ranges were coded as ‘uncertain’ to incorporate the uncertainty associated with the climatic distribution of such species. Maximum likelihood reconstruction of ancestral niches was performed using the nichevol R package (version 0.1.20; https://github.com/marlonecobos/nichevol.git) [101]. Based on the BR character codes for a given bin of environmental values, the niche evolution was assessed as follows [9,14]: (1) presence in ancestor and absence in descendent is identified as retraction, (2) absence in the ancestor and presence in the descendent is identified as expansion, and (3) maintenance of identical states in ancestor and descendant, and no indication of changes due to the uncertainty of environmental utilization in ancestor and/or descendent, is termed as stasis (i.e., no change). If the current niche of the descendent species exceeds the upper limit of its ancestral niche, the niche change is termed as ‘expansion high’, and if the current niche range exceeds the lower limit of its ancestral niche, it is ‘expansion low’. Similarly, if the niche of the descendent species retracts from the upper limit of its ancestral niche, it is ‘retraction high’, and if the retraction occurs at the lower limit, it is ‘retraction low’. For the currently-known species that experienced niche changes, ancestral niches, niche evolution, and current niches were represented in geographic space within the corresponding accessible areas. Boxplots were developed using the ggplot2 R package [102] to represent the ranges of environmental values at which the evolution occurred.
Results
Nearly half of the taxa experience thermal niche evolution
We analyzed the utilization of the temperature variable by each of the species (i.e., the realized temperature niche) (S3 Table; S1 Fig.). At the lower-limit spectrum, G. hossei utilized the lowest temperature (1.5oC), and G. stenopleurum, the highest (24.3oC), whereas, on the higher-limit spectrum, the lowest temperature (14.2oC) was used by G. reductum, and the highest limit (25.4oC) was occupied by both G. eurypleurum and G. stenopleurum. Gymnocalycium mesopotamicum used the lowest range of temperature (0.5oC), and G. marsoneri, the widest (18.2oC). In the simulated accessible areas, the minimum width of temperature range was observed for both G. mesopotamicum and G. stenopleurum (1.1oC), and the maximum width was noted for G. hossei (29.5oC).
Nearly half of the species (17/40) in the Gymnocalycium clade experienced changes in temperature niches over time. Both expansion and retraction events were noted across the phylogeny (Fig 3). The thermal niches of G. saglionis, G. ritterianum, G. bruchii, G. paraguayense, and G. mihanovichii were only expanded with respect to that of their ancestors. The niche expansion events in G. spegazzinii and G. schickendantzii were also accompanied by niche retractions. No ancestral temperature niches were retained by G. schickendantzii. Gymnocalycium castellanosii, G. rhodantherum, G. pugionacanthum, G. bodenbenderianum, G. mesopotamicum, G. calochlorum, G. striglianum, G. reductum, G. marsoneri, and G. pflanzii experienced only niche retractions. With reference to the Ms, we estimated the utilization of temperature niches by ancestors and descendants (S2 Fig.). The thermal niche expansion at the upper end of the ancestral niche limit was noted only for G. paraguayense, whereas, all other expansion events occurred at the lower limits. The upper limits of the ancestral niches were retracted for G. rhodantherum, G. spegazzinii, G. reductum, G. striglianum, and G. pflanzii; for the remaining species, niche retractions were at the lower limits, except for G. mesopotamicum and G. marsoneri, for which complete niche retractions with respect to the ancestral conditions were noted; however, for these species, the ancestral thermal niches corresponding to the current conditions were uncertain (Fig 3). The ancestral niches, niches of descendant species, and niche changes were represented in the geographic space (S3 Fig.). We noted that most of the upper limit retraction events were reflected geographically at the eastern side of the species’ current distributions. Mixed geographic patterns were observed in other niche evolutionary events (i.e., expansions and lower limit retractions).
The upper panel shows the evolutionary dynamics of temperature niches across the Gymnocalycium phylogeny. The bottom panel indicates the bioregion-specific distribution of 17 Gymnocalycium species that experienced temperature niche evolution. The shapefiles of countries were sourced from DIVA-GIS (https://diva-gis.org), a free and open-source geographic information system.
Precipitation niches are retracting
The utilization of the precipitation variable by each of the Gymnocalycium species is given in figure S4 (i.e., the realized precipitation niche) (S3 Table). The lowest value of the precipitation within the lower-limit spectrum was used by G. bodenbenderianum (108 mm), and the highest value was noted for G. horstii (1534 mm). Gymnocalycium glaucum tolerated the lowest value of the precipitation (206 mm), and the utilization of the highest precipitation value (1813 mm) was observed for G. paraguayense, within the higher-limit spectrum of the precipitation values. Gymnocalycium glaucum used the narrowest precipitation range (77 mm), and G. schroederianum, the highest (840 mm). In the simulated Ms, the lowest range of precipitation values available for utilization was noted for G. glaucum (77 mm), and the widest range of values available for utilization was observed for G. marsoneri (1562 mm).
Precipitation niche evolution was noted in only ~23% (9/40) of the species in the Gymnocalycium clade (Fig 4). None of the species experienced niche expansion events. Niche retraction events were noted in G. castellanosii, G. spegazzinii, G. hyptiacanthum, G. mesopotamicum, G. bruchii, G. schroederianum, G. andreae, G. reductum, and G. eurypleurum. The upper limit of the ancestral precipitation niche was retracted only in G. castellanosii, and the lower limit retraction was noted in G. reductum. All other species experienced complete precipitation niche retractions (S5 Fig.); however, the ancestral precipitation niches corresponding to the current conditions were uncertain in those species (Fig 4). The geographic representation of the niche evolutionary events revealed that the retraction at the upper-limit caused range contraction at the eastern side of the species’ current distribution (S6 Fig.).
The upper panel shows the evolutionary dynamics of precipitation niches across the Gymnocalycium phylogeny. The bottom panel indicates the bioregion-specific distribution of nine Gymnocalycium species that experienced precipitation niche evolution. The shapefiles of countries were sourced from DIVA-GIS (https://diva-gis.org), a free and open-source geographic information system.
Among the species that experienced niche evolutionary changes, five species, viz., G. bruchii, G. castellanosii, G. mesopotamicum, G. reductum, and G. spegazzinii, were noted for evolving niches in both environmental dimensions (Table 1; Figs 3–4).
Bioregion-specific evolutionary trends are prevailing
The biogeographic classification of this region comprises three dominions: Chacoan dominion (CD), Paraná dominion (PD), South Brazilian dominion (SBD), and the South American transition zone (SATZ) (Table 1). No evolutionary changes in precipitation niches were detected for species, distributed either partly or fully, within the South Brazilian dominion (Table 1; Fig 4). Among these, G. pflanzii is the only species well distributed in the SBD that experienced thermal niche evolution. Other species, such as G. marsoneri, G. saglionis, and G. schickendantzii, also underwent changes in thermal niches but showed sparse distribution within the SBD. In contrast, other well distributed species within this dominion, such as G. baldianum, G. bayrianum, and G. oenanthemum, have conserved both their thermal and precipitation niches. Gymnocalycium denudatum, G. hyptiacanthum and G. schroederianum are partially distributed in the Paraná dominion. The thermal niches of these species have been phylogenetically conserved; however, the precipitation niches have evolved in G. hyptiacanthum and G. schroederianum. Most of the Gymnocalycium species (80%; 32/40) have their distribution either fully or partly in the Chacoan dominion. Except for G. spegazzinii, the remaining eight species that experienced changes in the precipitation niches were distributed either partly (G. andreae, G. bruchii, G. castellanosii, G. hyptiacanthum, and G. schroederianum), or fully (G. eurypleurum, G. mesopotamicum, and G. reductum) in the CD. Among the 17 species, for which the thermal niches have evolved, G. calochlorum, G. mesopotamicum, G. mihanovichii, G. paraguayense, and G. reductum were distributed only in the CD, and the distribution of G. striglianum, G. pugionacanthum, G. rhodantherum, and G. spegazzinii were restricted only to the SATZ. Thermal niche expansion at the upper limit of the ancestral niche was noticed only in G. paraguayense distributed in the CD. No strict patterns of niche evolution were observed with regard to the altitudinal gradients (S7 Fig.); however, the width of altitudinal gradient (WAG) for all species that experienced changes in the precipitation niches was noted to be ≤ 1500 m, and 78% (7/9) of the species with precipitation niche changes were distributed at altitudes less than 2000 m.
Niche changes at the interface of paleoclimatic changes
Most of the diversification events in the Gymnocalycium clade occurred within the last one million years (0.03–0.95 Mya; S8 Fig.), coinciding with the Middle and Early Patagonian glaciations, however, two exceptions, G. saglionis (~3.79 Mya) and G. paraguayense (~1.45 Mya), diverged earlier, prior to the Great Patagonian Glaciations (GPG: 1.0–1.1 Mya). These species experienced thermal niche changes only, with both showing evidence of niche expansion. All species that experienced evolution in their precipitation niches diverged in the last one million years. Within the spectrum of Early–Middle Pleistocene glaciations in this region, most of the niche changes in both temperature and precipitation dimensions, either retraction or expansion, occurred in the Post-GPG 2 phase (> 0.128 to < 0.710 Mya) (S8 Fig.). In the temperature dimension, the Gymnocalycium species that diversified during the Post-GPG 1 phase (> 0.710 to < 1.0 Mya) experienced either upper-limit retraction (G. pflanzii, ~ 0.95 Mya), or complete-non-utilization of environmental values (G. schickendantzii, ~ 0.78 Mya) with respect to that of their ancestors. Nonetheless, G. schickendantzii also experienced thermal niche expansion at the lower limit. Another species that diverged during Post-GPG 1 phase experienced complete-non-utilization of ancestral conditions, was G. mesopotamicum; however, the estimation of ancestral conditions for this species involved uncertainties. Half of the species (50%; 4/8) that diverged during the Post-GPG 2 phase underwent thermal niche retractions at the lower limits: G. bodenbenderianum (~0.20 Mya), G. calochlorum (~0.25 Mya), G. pugionacanthum (~0.50 Mya), and G. castellanosii (~0.51 Mya). A complete retraction of ancestral conditions with wide ranges of uncertainty in ancestral niches was noted in G. marsoneri (~0.39 Mya; Post-GPG 2). Either lower-limit expansion (G. ritterianum, ~ 0.04 Mya), or upper-limit retraction (G. rhodantherum, 0.04 Mya; G. striglianum, ~ 0.04 Mya; G. reductum, ~ 0.07 Mya) was observed in species that diverged during the Post-GPG 3 phase (Upper/Late Middle Pleistocene glaciations, < 0.128 Mya).
In the precipitation dimension, a complete-non-utilization of ancestral niches was noted in G. hyptiacanthum and G. mesopotamicum that diverged during the Post-GPG 1 phase. Similarly, a full retraction of ancestral niches was noted in the species diverged during the Post-GPG 2 phase, except for G. castellanosii that experienced upper limit retraction. A complete-non-utilization of ancestral conditions was noted in G. andreae (~0.09 Mya), and lower-limit retraction was observed in G. reductum (~0.07 Mya), diverged during the Post-GPG 3 phase. However, irrespective of the times of divergence, significant portions of the reconstructed ancestral precipitation niches of the species for which a complete-non-utilization of ancestral niches was noted were uncertain. Among the five species that experienced evolution in both temperature and precipitation dimensions, three diverged in the Post-GPG 2 phase: G. bruchii (~0.46 Mya), G. spegazzinii (~0.50 Mya), and G. castellanosii (~0.51 Mya).
Discussion
Retrospection: what, why and how?
Recent years have witnessed researchers using various methods and tools to reconstruct the ancestral niches [9]. The main shortfall of all such methods stems from the basic fact that it is difficult to estimate the fundamental niche of a species from the presence points alone [9]. Studies that used the summary statistics based on presence points alone pose higher risk of biased sampling, as the occurrence abundance of a species in a particular environment cannot always be interpreted that this suite of environmental conditions are highly favourable for the given species [9]. Because the observed abundance could be due to either biased sampling, or that it may be the most common environment in the accessible area. The BAR method stands out from the methods outlined [9] for two major reasons: the inclusion of the accessible area hypothesis in the analysis and the explicit incorporation of uncertainty. The methods that do not consider these two factors may produce results at the cost of over- or under-estimation of the true niche changes over time across the phylogeny [8]. The BAR method considers ranged response instead of a single value (median values of variables based on realized niche) which is used in more traditional generalized least squares reconstruction (GLS) approaches to estimate ecological niches. Hence, a potential limitation of the BAR method is the lack of an approach for the quantitative estimation of niche evolutionary rates that are comparable to the rates estimated from the conventional single-value reconstructions [9].
For the first time, our study reveals the evolutionary dynamics of the climatic niches of Gymnocalycium species in detail with respect to their ancestors, integrating a dated phylogeny. In plants, this approach (i.e., BAR method) was earlier used by Ashraf et al. [16] to decipher the patterns of niche conservatism and evolution in the members of the Oleaceae family. Several other studies on plants, in which climatic niche evolution was investigated across phylogenies using different approaches [103–111], did not specifically incorporate an accessible area hypothesis for the extant species [7,9,83,84], and the inherent uncertainties associated with the incomplete characterization of fundamental niches (i.e., full niche ranges of extant species) [8,9]—the two interlinked and indispensable, yet often overlooked, components in the ancestral niche reconstruction workflows [9]. Hence, a clear depiction of the niche evolutionary dynamics (uncertainty, expansion, retraction, and/or stasis) in terms of the utilization of environmental values and the representation of such dynamics within the accessible areas of extant species, with respect to their ancestors, were also lacking in the above studies. In contrast, with the support of well-defined accessible area hypotheses for each of the Gymnocalycium species, we investigated four questions that paved the way for new valid insights on: 1) species’ tendencies to conserve/evolve their niches over time, 2) variable-wise differences in the evolutionary dynamics, 3) bioregion specificities in the patterns of niche conservatism and/or evolution, 4) the role of paleo-climatic events on niche divergences, 5) niche evolution within the accessible areas, and 6) the need for species-specific and region-specific conservation efforts, by characterizing the niches of both extant species and their ancestors in two environmental dimensions (i.e., temperature and precipitation variables), specifically incorporating the ‘uncertainty component’.
Not very strict, but alarming
We observed clear evolutionary trends in both thermal and precipitation dimensions across the Gymnocalycium phylogeny; however, we also observed a relatively high, though not strict, conservation of precipitation niches. Cactaceae species are distributed mostly in arid environments, and their roots are specialized to extract water in precipitation-deficit conditions [112]. The roots of Gymnocalycium species experience evolution; basal lineages possess fascicular roots and terminal clades have napiform roots [69]. Fascicular roots facilitate the intake of water from shallow soils [113], and napiform roots help to store water to tolerate severe drought [114]. The tendency to conserve precipitation niche was more evident in species with fascicular roots than in those with napiform roots, as only three out of twenty-three species with fascicular root system experienced niche evolution with respect to precipitation dimension (viz., G. castellanosii, G. eurypleurum, and G. spegazzinii), whereas all remaining species that experienced changes in precipitation niche possess napiform root system [69]. We find this trend alarming because Gymnocalycium species with fascicular roots (see S1 Table for details) may be more sensitive to climate change, as superficial roots are highly sensitive to increases in soil temperatures [115,116]. In addition, climate change can cause these superficial roots to experience elevated respiration rates, and it may also result in reduced storage of water in shallow soil after rainfall events [112]. Hence, the populations of Gymnocalycium species with fascicular roots, that are distributed on the hot and dry limits of their ranges may face serious threats in a warming climate, leading to the contraction of their geographic ranges [112]. Non-adaptability to changing environments is the main reason behind the rise of species conservation issues, and such failures in adaptation largely represent cases of niche conservatism [117]. Ecophysiological studies that link the responses of these Gymnocalycium species to high temperatures may provide more insights on their thermal tolerances [118–120]. No expansion in precipitation niches further confirms the possibility of range contractions. Recently, Ringelberg et al. [121] reported conservation of precipitation niches across phylogeny in a large group of plants (Mimosoid legumes), and suggested that this phylogenetic niche conservatism is a major factor behind speciation in that group. Even so, we refrain from stating that the prevalence of high precipitation niche conservatism (>75%) is a major factor behind the speciation in Gymnocalycium group, as the evidence of niche conservatism across the phylogeny does not necessarily prove or disprove its role in lineage divergence [103] because speciation involves multiple stages [122].
Bioregion-specific conservation practices
Bioregion-specific patterns were noted in the niche changes in Gymnocalycium. Based on the globally assigned aridity index (AI) values [123], the distributional patterns of Gymnocalycium species encompass arid, semi-arid, dry sub-humid, and humid ranges (see [124], for details). The increase in humidity follows an eastward longitudinal pattern [124]. A high density of species composition exists in the western part of the current Gymnocalycium distribution, particularly in the SATZ, SBD, and CD, experiencing arid to semi-arid conditions. The Gymnocalycium species with conserved precipitation niches, possessing fascicular roots and distributed in these regions, may require special attention, as global warming can induce serious threats to such species assemblages. Not to overlook, the species distributed in the eastern part are not completely free from the threats, as global warming could cause a 56% expansion of dryland area by the end of this century [124,125].
Pleistocene glaciations, speciation, and niche evolution
Freezing climatic conditions during the Pre-GPG, and three Post-GPGs in particular, might be the major driving force behind the lineage divergence events in the Gymnocalycium clade. In Cactaceae, a recent study [126] demonstrated that Pleistocene glaciations influenced speciation processes in the genus Eriosyce, using genetic data and species distribution models developed for present and past conditions. Cactus species are highly adapted to water-limiting condition [127]. Extreme cold conditions could affect the efficiency of cactus roots to extract water from soil, may be, in two ways: cell ruptures can occur due to the internal formation of ice crystals [128], and soil water conductivity becomes extremely low below 0oC [129]. These factors may be linked directly to why cactus distribution is restricted in freezing environments [130], although the lethality of extreme cold conditions does vary among different cactus species [131]. As an obvious non-preference for extreme cold conditions, the western limit of the current distribution of Gymnocalycium species is slightly shifted away from the eastern edges of the glaciers [132,133]. We assume that even though Gymnocalycium species are drought resistant, the surface water availability (shallow moisture content) could be a crucial driver in their distribution, underpinned by the observation that most species tend to conserve their precipitation niches. This is further supported by the facts that small precipitation pulses translate to shallow soil moisture content [134], and the sensitivity of the shallow root system of cactus species to low precipitation events is a function that facilitate the development of main roots [112,135,136]. The tropical niche conservatism hypothesis [137,138] supports the fact that plants in the Neotropical region tend to conserve their niches over time [139]. Following the diversification events in the Early–Middle Pleistocene glaciations, we presume that the Gymnocalycium species might have followed a relatively ‘more tight-less tight’ pattern in retaining the ancestral niche characteristics related to the precipitation and temperature variables, respectively; probably as an ecological strategy for conserving the critical variable at the expense of the other [41,140]. Species tend to adopt ecological strategies against evolutionary pressures within their habitats, and such strategies are shaped by the environment [141]. The prevalence of both expansion and retraction events in the temperature niches (i.e., more labile), along with only retraction events in the precipitation niches, further strengthens our assumptions. In addition, a recent study revealed that the seed mass of Gymnocalycium species is related to climatic variables, precipitation in particular [142]. Although Gymnocalycium species are distributed in arid environments, their study found that the precipitation variable is important in the early stages of growth in Gymnocalycium species, adding support to the observed phenomenon of conservatism in the precipitation variable.
Conclusion
Our study provides new insights into the evolutionary dynamics of climatic niches within the genus Gymnocalycium, highlighting both the stability and adaptability of these species in response to environmental changes over time. By examining the phylogenetic evolution of niches with robustly defined accessible area hypotheses, we have elucidated patterns of niche conservatism and variability in temperature and precipitation across bioregions, highlighting the unique vulnerability of Gymnocalycium species with fascicular roots. These results show that while these cacti tend to conserve their precipitation niches, they are likely to face significant challenges in a warmer climate, particularly species from arid regions with shallow root systems. Furthermore, Pleistocene glaciations appear to have shaped the evolutionary trajectories of Gymnocalycium, contributing to lineage divergence and niche specialization. Finally, our results highlight the importance of conservation strategies that address bioregion-specific challenges, especially as climate change threatens to alter the distribution and survival of these ecologically distinctive cacti. For the Gymnocalycium species distributed mostly in the mountain regions, in situ conservation programs may not serve the long-term goal. It is not possible for these species to simply move up and down the mountains to mitigate the climate change impacts, as land availability and dispersal capabilities are limited. Most of these species utilize specific climatic bands along elevational gradients. Therefore, future research that focuses on predicting the potential distribution of Gymnocalycium species in different periods (e.g., 2040, 2070, and 2100) under different scenarios of greenhouse gas emissions will help decide the viability of species-based in situ conservation strategies, utility of ex situ conservation efforts, and possibility of translocating plants from their current habitat to potential distribution areas on a timely basis, considering the climatic impacts.
Supporting information
S1 Fig. Available and occupied temperature ranges Temperature ranges based on the accessible areas represent available conditions, and those based on occurrence records represent ranges occupied by the species.
https://doi.org/10.1371/journal.pone.0323758.s001
(PDF)
S2 Fig. Graphical representation of temperature niche changes.
The niche evolutionary events (i.e., retraction and/or expansion) at the upper and/or lower limits with respect to the ancestral niches are represented within the accessible areas (M) of 16 Gymnocalycium species. No ancestral ranges were plotted for G. paraguayense and G. schickendantzii, as their ancestors did not utilize the temperature ranges within their M-areas. No graph was plotted for G. mesopotamicum, as the predicted retraction fell outside the available temperature limits of its M-area.
https://doi.org/10.1371/journal.pone.0323758.s002
(PNG)
S3 Fig. Geographic representation of temperature niche changes.
The predicted niche evolutionary events (i.e., retraction and/or expansion) are represented in geographic space. For each species, the ancestral niche, evolutionary changes, and present niche are depicted geographically within the accessible areas (M).
https://doi.org/10.1371/journal.pone.0323758.s003
(PNG)
S4 Fig. Available and occupied precipitation ranges.
Precipitation ranges based on the accessible areas represent available conditions, and those based on occurrence records represent ranges occupied by the species.
https://doi.org/10.1371/journal.pone.0323758.s004
(PDF)
S5 Fig. Graphical representation of precipitation niche changes.
The niche evolutionary events (i.e., retraction and/or expansion) at the upper and/or lower limits with respect to the ancestral niches are represented within the accessible areas (M) of six Gymnocalycium species. No graph was plotted for G. mesopotamicum, as the predicted retraction fell outside the available precipitation limits of its M-area.
https://doi.org/10.1371/journal.pone.0323758.s005
(PNG)
S6 Fig. Geographic representation of precipitation niche changes.
The predicted niche evolutionary events (i.e., retraction and/or expansion) are represented in geographic space. For each species, the ancestral niche, evolutionary changes, and present niche are depicted geographically within the accessible areas (M).
https://doi.org/10.1371/journal.pone.0323758.s006
(PNG)
S7 Fig. Altitudinal gradients.
The distribution of the Gymnocalycium species across the altitudinal gradient. The colors indicate the evolutionary specificities with respect to the temperature and precipitation dimensions. TNE - Temperature niche evolution, PNE - Precipitation niche evolution, and Both - Niche evolution in both dimensions.
https://doi.org/10.1371/journal.pone.0323758.s007
(PNG)
S8 Fig. Dated phylogenetic tree.
The Bayesian evolutionary tree representing the relationship between the Gymnocalycium species, and their divergence time estimates. The green numerals indicate the divergence time estimates of Gymnocalycium species. The branch colors represent the evolutionary specificities with respect to the temperature and precipitation dimensions. Divergence time estimates are in millions of years.
https://doi.org/10.1371/journal.pone.0323758.s008
(PNG)
S1 Table. Distributional information.
Details of species used in the present study, and corresponding root systems.
https://doi.org/10.1371/journal.pone.0323758.s009
(XLSX)
S2 Table. Parameter settings.
Parameterization of the M simulations in the grinnell R package. Simulations were performed for the current scenario (1979–2013).
https://doi.org/10.1371/journal.pone.0323758.s010
(DOCX)
S3 Table. Binning.
Descriptive statistics of temperature and precipitation variables, and associated bins.
https://doi.org/10.1371/journal.pone.0323758.s011
(XLSX)
Acknowledgments
The first author would like to thank the National Scientific and Technical Research Council (CONICET) of Argentina for providing a scholarship.
References
- 1. Freilij D, Larrea‐Alcazar D, Lopez RP, Velarde Simonini F, Naoki K, Bessega C. Environmental gradualism explains variation in pollination systems of columnar cacti: phylogenetic and trait evolution analyses. Glob Ecol Biogeogr. 2023;32:1015–29.
- 2. Aquino D, Moreno-Letelier A, González-Botello MA, Arias S. The importance of environmental conditions in maintaining lineage identity in Epithelantha (Cactaceae). Ecol Evol. 2021;11(9):4520–31. pmid:33976827
- 3. Amaral DT, Minhós‐Yano I, Oliveira JVM, Romeiro‐Brito M, Bonatelli IAS, Taylor NP, et al. Tracking the xeric biomes of South America: The spatiotemporal diversification of Mandacaru cactus. Journal of Biogeography. 2021;48(12):3085–103.
- 4. Thompson JB, Hernández-Hernández T, Keeling G, Vásquez-Cruz M, Priest NK. Identifying the multiple drivers of cactus diversification. Nat Commun. 2024;15(1):7282. pmid:39179557
- 5. Colwell R, Fuentes E. Experimental studies of the niche. Annu Rev Ecol Syst. 1975;6:281–310.
- 6. Peterson AT. Ecological niche conservatism: a time-structured review of evidence. Journal of Biogeography. 2011;38(5):817–27.
- 7. Soberon J, Peterson AT. Interpretation of Models of Fundamental Ecological Niches and Species’ Distributional Areas. Biodiv Inf. 2005;2(0).
- 8. Saupe EE, Barve N, Owens HL, Cooper JC, Hosner PA, Peterson AT. Reconstructing Ecological Niche Evolution When Niches Are Incompletely Characterized. Syst Biol. 2018;67(3):428–38. pmid:29088474
- 9. Owens HL, Ribeiro V, Saupe EE, Cobos ME, Hosner PA, Cooper JC, et al. Acknowledging uncertainty in evolutionary reconstructions of ecological niches. Ecol Evol. 2020;10(14):6967–77. pmid:32760505
- 10. Soberón J, Peterson AT. What is the shape of the fundamental Grinnellian niche? Theor Ecol. 2019;13(1):105–15.
- 11. Cooper N, Freckleton RP, Jetz W. Phylogenetic conservatism of environmental niches in mammals. Proc Biol Sci. 2011;278(1716):2384–91. pmid:21208967
- 12. Nyári ÁS, Reddy S. Comparative phyloclimatic analysis and evolution of ecological niches in the scimitar babblers (Aves: Timaliidae: Pomatorhinus). PLoS One. 2013;8(2):e55629. pmid:23405183
- 13. Pyron RA, Costa GC, Patten MA, Burbrink FT. Phylogenetic niche conservatism and the evolutionary basis of ecological speciation. Biol Rev Camb Philos Soc. 2015;90(4):1248–62. pmid:25428167
- 14. Cobos ME, Cheng Y, Song G, Lei F, Peterson AT. New distributional opportunities with niche innovation in Eurasian snowfinches. Journal of Avian Biology. 2021;52(12).
- 15. Engler JO, Lawrie Y, Cabral JS, Lens L, Martínez‐Meyer E. Niche evolution reveals disparate signatures of speciation in the ‘great speciator’ (white‐eyes, Aves: Zosterops). Journal of Biogeography. 2021;48(8):1981–93.
- 16. Ashraf U, Peterson AT, Chaudhry MN, Cobos ME. Global ecological niche conservatism and evolution in Olea species. Saudi J Biol Sci. 2023;30(1):103500. pmid:36458099
- 17. Mourelle C, Ezcurra E. Species richness of Argentine cacti: A test of biogeographic hypotheses. J Vegetation Science. 1996;7(5):667–80.
- 18. Godínez–Álvarez H, Valverde T, Ortega–Baes P. Demographic Trends in the Cactaceae. The Botanical Review. 2003;69(2):173–203.
- 19.
Fleming TH, Valiente-Banuet A. Columnar cacti and their mutualists: evolution, ecology, and conservation. University of Arizona Press; 2002.
- 20. Nobel PS. Morphology, Surface Temperatures, and Northern Limits of Columnar Cacti in the Sonoran Desert. Ecology. 1980;61(1):1–7.
- 21. Gurvich DE, Zeballos SR, Demaio PH. Diversity and composition of cactus species along an altitudinal gradient in the Sierras del Norte Mountains (Córdoba, Argentina). South African Journal of Botany. 2014;93:142–7.
- 22. Martorell C, Patiño P. Globose cacti (Mammillaria) living on cliffs avoid high temperatures in a hot dryland of Southern Mexico. Journal of Arid Environments. 2006;67(4):541–52.
- 23. Cavalcante AMB, Sampaio ACP, Duarte AS, Santos MAFD. Impacts of climate change on the potential distribution of epiphytic cacti in the Caatinga biome, Brazil. An Acad Bras Cienc. 2023;95(2):e20200904. pmid:37255123
- 24. Edwards EJ, Donoghue MJ. Pereskia and the origin of the cactus life-form. Am Nat. 2006;167(6):777–93. pmid:16649155
- 25. Pillet M, Goettsch B, Merow C, Maitner B, Feng X, Roehrdanz PR, et al. Elevated extinction risk of cacti under climate change. Nat Plants. 2022;8(4):366–72. pmid:35422081
- 26. Roberts D, Hamann A. Predicting potential climate change impacts with bioclimate envelope models: a palaeoecological perspective. Glob Ecol Biogeogr. 2012;21:121–33.
- 27. Sinervo B, Méndez-de-la-Cruz F, Miles DB, Heulin B, Bastiaans E, Villagrán-Santa Cruz M, et al. Erosion of lizard diversity by climate change and altered thermal niches. Science. 2010;328(5980):894–9. pmid:20466932
- 28.
Kiesling R, Larrocca L, Faúndez J, Metzing D, Albesiano S. Cactaceae . In: Zuolaga FO, Morrone O, and Belgrano MJ, editors. Catálogo de las Plantas Vasculares del Cono Sur. Monographs in Systematic Botany from the Missouri Botanical Garden 107, Saint Louis; 2008. p. 1715–1830.
- 29.
Charles GJ. Gymnocalycium in habitat and culture. Stamford: G. Charles; 2009.
- 30. Martino PA, Bauk K, Ferrero MC, Gurvich DE, Las Peñas ML. Ecological significance of determinate primary root growth: inter- and intra-specific differences in two species of Gymnocalycium (Cactaceae) along elevation gradients. Flora. 2018;248:70–5.
- 31. Bauk K, Gurvich DE, Las Peñas ML. Cytogenetic Characteristics of Four Gymnocalycium (Cactaceae) Species along Altitudinal Gradients. Haseltonia. 2023;29(1).
- 32. Martino P, Gurvich ED, Las Peñas ML. DNA content and cytogenetic characteristics of Gymnocalycium quehlianum (Cactaceae) Along An altitudinal gradient. BAG. 2022;33(1):51–9.
- 33. Gurvich DE, Demaio P, Giorgis MA. The diverse globose cactus community of Argentina’s Sierras ChicasEcology and conservation. Cactus and Succulent Journal. 2006;78(5):224–30.
- 34. Gurvich DE, Lorenzati MA, Sosa-Pivatto M, Bauk K, Barroso FL. Effects of long-term seed storage on germination of 13 cactus species from central Argentina. Journal of Arid Environments. 2021;185:104382.
- 35. Oyarzabal M, Clavijo J, Oakley L, Biganzoli F, Tognetti P, Barberis I. Vegetation units of Argentina. Ecol Austral. 2018;28.
- 36. Perotti SB, Aliscioni NL, Delbón NE, Perea M, Hammann A, Gurvich DE. Biomass Partitioning and Morphoanatomical Traits of Six Gymnocalycium (Cactaceae) Species Occurring along a Precipitation Gradient. Diversity. 2022;14(9):749.
- 37. Bauk K, Pérez-Sánchez R, Zeballos SR, Las Peñas ML, Flores J, Gurvich DE. Are seed mass and seedling size and shape related to altitude? Evidence in Gymnocalycium monvillei (Cactaceae). Botany. 2015;93(8):529–33.
- 38. Bauk K, Flores J, Ferrero C, Pérez-Sánchez R, Las Peñas ML, Gurvich DE. Germination characteristics of Gymnocalycium monvillei (Cactaceae) along its entire altitudinal range. Botany. 2017;95(4):419–28.
- 39. Janzen D. Why mountain passes are higher in the tropics. Am Nat. 1967;101:233–49.
- 40. Stevens GC. The latitudinal gradient in geographical range: how so many species coexist in the tropics. Am Nat. 1989;133:240–56.
- 41. Ackerly D. Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci. 2003;164:S165–84.
- 42. Janz N, Nylin S. The oscillation hypothesis of host-plant range and speciation. Speciation and Radiation: Evolutionary Biology of Herbivorous Insects. 2008;2008:203–15.
- 43. Wilson EO. The Nature of the Taxon Cycle in the Melanesian Ant Fauna. The American Naturalist. 1961;95(882):169–93.
- 44. Lancaster LT. On the macroecological significance of eco-evolutionary dynamics: the range shift-niche breadth hypothesis. Philos Trans R Soc Lond B Biol Sci. 2022;377(1846):20210013. pmid:35067095
- 45. Botts EA, Erasmus BFN, Alexander GJ. Small range size and narrow niche breadth predict range contractions in South African frogs. Global Ecology and Biogeography. 2012;22(5):567–76.
- 46. Pither J. Climate tolerance and interspecific variation in geographic range size. Proc Biol Sci. 2003;270(1514):475–81. pmid:12641901
- 47. Sheth SN, Morueta-Holme N, Angert AL. Determinants of geographic range size in plants. New Phytol. 2020;226(3):650–65. pmid:31901139
- 48. Slatyer RA, Hirst M, Sexton JP. Niche breadth predicts geographical range size: a general ecological pattern. Ecol Lett. 2013;16(8):1104–14. pmid:23773417
- 49. Yu F, Groen TA, Wang T, Skidmore AK, Huang J, Ma K. Climatic niche breadth can explain variation in geographical range size of alpine and subalpine plants. International Journal of Geographical Information Science. 2016;31(1):190–212.
- 50. Fisher-Reid MC, Kozak KH, Wiens JJ. How is the rate of climatic-niche evolution related to climatic-niche breadth? Evolution. 2012;66(12):3836–51. pmid:23206141
- 51. Quintero I, Wiens JJ. Rates of projected climate change dramatically exceed past rates of climatic niche evolution among vertebrate species. Ecol Lett. 2013;16(8):1095–103. pmid:23800223
- 52. Title PO, Burns KJ. Rates of climatic niche evolution are correlated with species richness in a large and ecologically diverse radiation of songbirds. Ecol Lett. 2015;18(5):433–40. pmid:25808028
- 53. Gurvich DE, Pérez-Sánchez R, Bauk K, Jurado E, Ferrero MC, Funes G, et al. Combined effect of water potential and temperature on seed germination and seedling development of cacti from a mesic Argentine ecosystem. Flora. 2017;227:18–24.
- 54. Antonelli A. Biogeography: Drivers of bioregionalization. Nat Ecol Evol. 2017;1(4):114. pmid:28812664
- 55. Morrone JJ. Biogeographical regionalisation of the Neotropical region. Zootaxa. 2014;3782:1–110. pmid:24871951
- 56. Morrone JJ, Escalante T, Rodríguez-Tapia G, Carmona A, Arana M, Mercado-Gómez JD. Biogeographic regionalization of the Neotropical region: New map and shapefile. An Acad Bras Cienc. 2022;94(1):e20211167. pmid:35107518
- 57. Ahmadzadeh F, Flecks M, Carretero MA, Böhme W, Ilgaz C, Engler JO, et al. Rapid lizard radiation lacking niche conservatism: ecological diversification within a complex landscape. Journal of Biogeography. 2013;40(9):1807–18.
- 58. Castro-Insua A, Gómez-Rodríguez C, Wiens JJ, Baselga A. Climatic niche divergence drives patterns of diversification and richness among mammal families. Sci Rep. 2018;8(1):8781. pmid:29884843
- 59. Hua X, Wiens JJ. How does climate influence speciation?. Am Nat. 2013;182(1):1–12. pmid:23778222
- 60. Jezkova T, Wiens JJ. Testing the role of climate in speciation: New methods and applications to squamate reptiles (lizards and snakes). Mol Ecol. 2018;27(12):2754–69. pmid:29779234
- 61. Rato C, Harris DJ, Perera A, Carvalho SB, Carretero MA, Rödder D. A Combination of Divergence and Conservatism in the Niche Evolution of the Moorish Gecko, Tarentola mauritanica (Gekkota: Phyllodactylidae). PLoS One. 2015;10(5):e0127980. pmid:26000981
- 62.
Coronato A, Martínez O, Rabassa J. Glaciations in Argentine Patagonia, southern South America. Developments in Quaternary Sciences. Elsevier. 2004. p. 49–67. https://doi.org/10.1016/s1571-0866(04)80111-8
- 63. Rabassa J, Coronato A, Martinez O. Late cenozoic glaciations in patagonia and tierra del fuego: an updated review. Biol J Linn Soc. 2011;103:316–35.
- 64. Baranzelli MC, Cosacov A, Espíndola A, Iglesias M del R, Chan LM, Johnson LA, et al. Echoes of the whispering land: interacting roles of vicariance and selection in shaping the evolutionary divergence of two Calceolaria (Calceolariaceae) species from Patagonia and Malvinas/Falkland Islands. Evol Ecol. 2018;32(2–3):287–314.
- 65. Brusquetti F, Netto F, Baldo D, Haddad CFB. The influence of Pleistocene glaciations on Chacoan fauna: genetic structure and historical demography of an endemic frog of the South American Gran Chaco. Biological Journal of the Linnean Society. 2019;126(3):404–16.
- 66. Campagna L, St Clair JJH, Lougheed SC, Woods RW, Imberti S, Tubaro PL. Divergence between passerine populations from the Malvinas - Falkland Islands and their continental counterparts: a comparative phylogeographical study. Biol J Linn Soc Lond. 2012;106(4):865–79.
- 67. Cosacov A, Sérsic AN, Sosa V, Johnson LA, Cocucci AA. Multiple periglacial refugia in the Patagonian steppe and post‐glacial colonization of the Andes: the phylogeography of Calceolaria polyrhiza. Journal of Biogeography. 2010;37(8):1463–77.
- 68. Ortiz-Jaureguizar E, Cladera GA. Paleoenvironmental evolution of southern South America during the Cenozoic. Journal of Arid Environments. 2006;66(3):498–532.
- 69. Demaio PH, Barfuss MHJ, Kiesling R, Till W, Chiapella JO. Molecular phylogeny of Gymnocalycium (Cactaceae): assessment of alternative infrageneric systems, a new subgenus, and trends in the evolution of the genus. Am J Bot. 2011;98(11):1841–54. pmid:22012926
- 70.
GBIF.org. GBIF Occurrence Download; (13 November 2024). https://doi.org/10.15468/dl.e4j676
- 71. Meregali M, Metzing D, Kiesling R, Tosatto S, Caramiello R. Systematics of the Gymnocalycium paraguayense-fleischerianum group (cactaceae): morphological and molecular data. Candollea. 2002;57:299–315.
- 72.
Pin AB, Pallisé JS. Guía ilustrada de los cactus del Paraguay. Asunción. Presidencia de la República. Secretaría del Ambiente; 2004.
- 73. Schedlich V, Wick M. The seeds of the genus Gymnocalycium. Part 4: Subgenus macrosemineum. Schütziana. 2020;11.
- 74.
QGIS.org. QGIS Geographic Information System. QGIS Association; 2024. Retrieved from: http://www.qgis.org
- 75. Aiello‐Lammens ME, Boria RA, Radosavljevic A, Vilela B, Anderson RP. spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography. 2015;38(5):541–5.
- 76. Brown JL, Hill DJ, Dolan AM, Carnaval AC, Haywood AM. PaleoClim, high spatial resolution paleoclimate surfaces for global land areas. Sci Data. 2018;5:180254. pmid:30422125
- 77. Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria-Auza RW, et al. Climatologies at high resolution for the earth’s land surface areas. Sci Data. 2017;4:170122. pmid:28872642
- 78. Booth TH. Checking bioclimatic variables that combine temperature and precipitation data before their use in species distribution models. Austral Ecology. 2022;47(7):1506–14.
- 79. Cuervo PF, Flores FS, Venzal JM, Nava S. Niche divergence among closely related taxa provides insight on evolutionary patterns of ticks. Journal of Biogeography. 2021;48(11):2865–76.
- 80. Díaz-Calafat J, Jaume-Ramis S, Soacha K, Álvarez A, Piera J. Revealing biases in insect observations: A comparative analysis between academic and citizen science data. PLoS One. 2024;19(7):e0305757. pmid:39024343
- 81. Escobar LE, Lira-Noriega A, Medina-Vogel G, Townsend Peterson A. Potential for spread of the white-nose fungus (Pseudogymnoascus destructans) in the Americas: use of Maxent and NicheA to assure strict model transference. Geospat Health. 2014;9(1):221–9. pmid:25545939
- 82. Nair RR, Gurvich DE, Pereyra M, Sérsic AN. Clandestine travelers, a boon for south and a bane for north? Warming-induced shifts in global invasion potential of Argentine ants. Biol Invasions. 2024;26(10):3369–92.
- 83. Barve N, Barve V, Jiménez-Valverde A, Lira-Noriega A, Maher SP, Peterson AT, et al. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling. 2011;222(11):1810–9.
- 84. Machado-Stredel F, Cobos ME, Peterson AT. A simulation-based method for selecting calibration areas for ecological niche models and species distribution models. Frontiers of Biogeography. 2021;13(4).
- 85. Feng X, Peterson AT, Aguirre-López LJ, Burger JR, Chen X, Papeş M. Rethinking ecological niches and geographic distributions in face of pervasive human influence in the Anthropocene. Biol Rev Camb Philos Soc. 2024;99(4):1481–503. pmid:38597328
- 86. Canham CD, Uriarte M. Analysis of neighborhood dynamics of forest ecosystems using likelihood methods and modeling. Ecol Appl. 2006;16(1):62–73. pmid:16705961
- 87. Greene DF, Canham CD, Coates KD, Lepage PT. An evaluation of alternative dispersal functions for trees. Journal of Ecology. 2004;92(5):758–66.
- 88.
Nathan R, Klein E, Robledo-Arnuncio JJ, Revilla E. Dispersal kernels: review. Clobert J, Baguette M, Benton TG, Bullock JM, editors. Dispersal Ecology and Evolution. Oxford University Press; 2012. pp. 186-210. https://doi.org/10.1093/acprof:oso/9780199608898.003.0015
- 89. Stoyan D, Wagner S. Estimating the fruit dispersion of anemochorous forest trees. Ecological Modelling. 2001;145(1):35–47.
- 90. Posada D. jModelTest: phylogenetic model averaging. Mol Biol Evol. 2008;25(7):1253–6. pmid:18397919
- 91. Drummond AJ, Ho SYW, Phillips MJ, Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006;4(5):e88. pmid:16683862
- 92. Gernhard T, Hartmann K, Steel M. Stochastic properties of generalised Yule models, with biodiversity applications. J Math Biol. 2008;57(5):713–35. pmid:18509650
- 93. Hernández-Hernández T, Brown JW, Schlumpberger BO, Eguiarte LE, Magallón S. Beyond aridification: multiple explanations for the elevated diversification of cacti in the New World Succulent Biome. New Phytol. 2014;202(4):1382–97. pmid:24611540
- 94. Drummond AJ, Suchard MA, Xie D, Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol. 2012;29(8):1969–73. pmid:22367748
- 95. Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA. Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7. Syst Biol. 2018;67(5):901–4. pmid:29718447
- 96.
Drummond AJ, Ho SY, Rawlence N, Rambaut A. A rough guide to BEAST 1.4. Auckland: University of Auckland; 2007.
- 97. Drummond AJ, Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol. 2007;7:214. pmid:17996036
- 98.
Rambaut A. FigTree. tree figure drawing tool. 2009. Retrieved from http://tree.bio.ed.ac.uk/software/figtree/
- 99. Lin L, Wiens JJ. Comparing macroecological patterns across continents: evolution of climatic niche breadth in varanid lizards. Ecography. 2016;40(8):960–70.
- 100. Ellepola G, Pie MR, Pethiyagoda R, Hanken J, Meegaskumbura M. The role of climate and islands in species diversification and reproductive-mode evolution of Old World tree frogs. Commun Biol. 2022;5(1):347. pmid:35411020
- 101. Cobos ME, Owens HL, Peterson AT. nichevol: Tools for ecological niche evolution assessment considering uncertainty. 2023. Available from: https://cran.r-project.org/web/packages/nichevol/index.html
- 102. Wickham H, Chang W, Henry L, Pedersen TL, Takahashi K, Wilke C, et al. ggplot2: Create elegant data visualisations using the grammar of graphics; 2024. Available from: https://cran.r-project.org/web/packages/ggplot2/index.html
- 103. Evans MEK, Smith SA, Flynn RS, Donoghue MJ. Climate, niche evolution, and diversification of the “bird-cage” evening primroses (Oenothera, sections Anogra and Kleinia). Am Nat. 2009;173(2):225–40. pmid:19072708
- 104. Koecke AV, Muellner-Riehl AN, Pennington TD, Schorr G, Schnitzler J. Niche evolution through time and across continents: The story of Neotropical Cedrela (Meliaceae). Am J Bot. 2013;100(9):1800–10. pmid:24018859
- 105. Liu H, Ye Q, Wiens JJ. Climatic-niche evolution follows similar rules in plants and animals. Nat Ecol Evol. 2020;4(5):753–63. pmid:32203479
- 106. Qi Z, Li P, Wu J, Gamisch A, Yang T, Zhao Y, et al. Climatic niche evolution in Smilacaceae (Liliales) drives patterns of species diversification and richness between the Old and New World. J of Sytematics Evolution. 2023;61(5):733–47.
- 107. Salariato DL, Zuloaga FO. Climatic niche evolution in the Andean genus Menonvillea (Cremolobeae: Brassicaceae). Org Divers Evol. 2016;17(1):11–28.
- 108. Smith SA, Beaulieu JM. Life history influences rates of climatic niche evolution in flowering plants. Proc Biol Sci. 2009;276(1677):4345–52. pmid:19776076
- 109. Smith SA, Donoghue MJ. Combining historical biogeography with niche modeling in the Caprifolium clade of Lonicera (Caprifoliaceae, Dipsacales). Syst Biol. 2010;59(3):322–41. pmid:20525639
- 110. Vasconcelos T, Boyko JD, Beaulieu JM. Linking mode of seed dispersal and climatic niche evolution in flowering plants. Journal of Biogeography. 2021;50(1):43–56.
- 111. Wang Q, Li Y, Zou D, Su X, Cai H, Luo A, et al. Phylogenetic niche conservatism and variations in species diversity–climate relationships. Ecography. 2021;44(12):1856–68.
- 112. Hultine KR, Hernández-Hernández T, Williams DG, Albeke SE, Tran N, Puente R, et al. Global change impacts on cacti (Cactaceae): current threats, challenges and conservation solutions. Ann Bot. 2023;132(4):671–83. pmid:36861500
- 113.
Gibson AC, Nobel PS. The cactus primer. Cambridge MA: Harvard University Press. 1986.
- 114.
Nobel PS. Cacti: biology and uses. Massachusetts: University of California Press; 2002.
- 115. Petrie MD, Bradford JB, Lauenroth WK, Schlaepfer DR, Andrews CM, Bell DM. Non-analog increases to air, surface, and belowground temperature extreme events due to climate change. Climatic Change. 2020;163(4):2233–56.
- 116. Schlaepfer DR, Bradford JB, Lauenroth WK, Munson SM, Tietjen B, Hall SA, et al. Climate change reduces extent of temperate drylands and intensifies drought in deep soils. Nat Commun. 2017;8:14196. pmid:28139649
- 117.
Holt R, Gomulkiewicz R. Conservation implications of niche conservatism and evolution in heterogeneous environments. In: Ferriere R, Dieckmann U, Couvet DD, editors. Evolutionary conservation biology. Cambridge: Cambridge University Press; 2004. p. 244 - 264.
- 118. Didden-Zopfy B, Nobel PS. High temperature tolerance and heat acclimation of Opuntia bigelovii. Oecologia. 1982;52(2):176–80. pmid:28310504
- 119. Smith SD, Didden-Zopfy B, Nobel PS. High‐Temperature Responses of North American Cacti. Ecology. 1984;65(2):643–51.
- 120. Ishikawa M, Gusta LV. Freezing and heat tolerance of Opuntia cacti native to the Canadian prairie provinces. Can J Bot. 1996;74(12):1890–5.
- 121. Ringelberg JJ, Koenen EJM, Sauter B, Aebli A, Rando JG, Iganci JR, et al. Precipitation is the main axis of tropical plant phylogenetic turnover across space and time. Sci Adv. 2023;9(7):eade4954. pmid:36800419
- 122. de Queiroz K. Ernst Mayr and the modern concept of species. Proc Natl Acad Sci U S A. 2005;102 Suppl 1(Suppl 1):6600–7. pmid:15851674
- 123.
Trabucco A, Zomer R. Global aridity index and potential evapotranspiration (ET0) climate database v2. figshare. 2019. https://doi.org/10.6084/m9.figshare.7504448.v3
- 124. Coleine C, Stajich JE, de Los Ríos A, Selbmann L. Beyond the extremes: Rocks as ultimate refuge for fungi in drylands. Mycologia. 2021;113(1):108–33. pmid:33232202
- 125.
Cherlet M, Hutchinson C, Reynolds J, Hill J, Sommer S, Von MG. World atlas of desertification: rethinking land degradation and sustainable land management. Luxembourg: Publication Office of the European Union; 2018.
- 126. Meriño BM, Villalobos-Barrantes HM, Guerrero PC. Pleistocene climate oscillations have shaped the expansion and contraction speciation model of the globose Eriosyce sect. Neoporteria cacti in Central Chile. Ann Bot. 2024;134(4):651–64. pmid:38824400
- 127. Bustamante E, Búrquez A. Effects of plant size and weather on the flowering phenology of the organ pipe cactus (Stenocereus thurberi). Ann Bot. 2008;102(6):1019–30. pmid:18854374
- 128. Flores F J-L, Yeaton RI. The replacement of arborescent cactus species along a climatic gradient in the southern Chihuahuan Desert: competitive hierarchies and response to freezing temperatures. Journal of Arid Environments. 2003;55(4):583–94.
- 129. Burt TP, Williams PJ. Hydraulic conductivity in frozen soils. Earth Surf Process. 1976;1(4):349–60.
- 130.
Levitt J. Responses of plants to environmental stress: chilling, freezing, and high temperature stresses. Academic Press. 1980.
- 131. Nobel PS. Low-Temperature Tolerance and Cold Hardening of Cacti. Ecology. 1982;63(6):1650.
- 132. Braun MH, Malz P, Sommer C, Farías-Barahona D, Sauter T, Casassa G, et al. Constraining glacier elevation and mass changes in South America. Nature Clim Change. 2019;9(2):130–6.
- 133. Dussaillant I, Berthier E, Brun F, Masiokas M, Hugonnet R, Favier V, et al. Two decades of glacier mass loss along the Andes. Nat Geosci. 2019;12(10):802–8.
- 134. Nano CEM, Pavey CR. Refining the ‘pulse‐reserve’ model for arid central Australia: Seasonal rainfall, soil moisture and plant productivity in sand ridge and stony plain habitats of the Simpson Desert. Austral Ecology. 2013;38(7):741–53.
- 135. Rodriguez-Alonso G, Matvienko M, López-Valle ML, Lázaro-Mixteco PE, Napsucialy-Mendivil S, Dubrovsky JG, et al. Transcriptomics insights into the genetic regulation of root apical meristem exhaustion and determinate primary root growth in Pachycereus pringlei (Cactaceae). Sci Rep. 2018;8(1):8529. pmid:29867103
- 136. Shishkova S, Las Peñas ML, Napsucialy-Mendivil S, Matvienko M, Kozik A, Montiel J, et al. Determinate primary root growth as an adaptation to aridity in Cactaceae: towards an understanding of the evolution and genetic control of the trait. Ann Bot. 2013;112(2):239–52. pmid:23666887
- 137. Wiens JJ. Global patterns of diversification and species richness in amphibians. Am Nat. 2007;170(Suppl)2:S86-106. pmid:17874387
- 138. Wiens JJ, Donoghue MJ. Historical biogeography, ecology and species richness. Trends Ecol Evol. 2004;19(12):639–44. pmid:16701326
- 139. Antonelli A, Sanmartín I. Why are there so many plant species in the Neotropics? TAXON. 2011;60(2):403–14.
- 140. Emery NC, Forrestel EJ, Jui G, Park MS, Baldwin BG, Ackerly DD. Niche evolution across spatial scales: climate and habitat specialization in California Lasthenia (Asteraceae). Ecology. 2012;93(sp8).
- 141. Southwood TRE, May RM, Hassell MP, Conway GR. Ecological Strategies and Population Parameters. The American Naturalist. 1974;108(964):791–804.
- 142. Bauk K, Rossi N, Gurvich DE, Las Peñas ML. Bioclimatic variables affect seed mass and seedling traits of four Gymnocalycium (Cactaceae) species along elevational gradients. Flora. 2025;322:152643.