Sympatric and allopatric niche shift of endemic Gypsophila (Caryophyllaceae) taxa in the Iberian Peninsula

Miguel de Luis; Carmen Bartolomé; Óscar García Cardo; Juan Manuel Martínez Labarga; Julio Álvarez-Jiménez

doi:10.1371/journal.pone.0206043

Abstract

Several species of the Gypsophila genus are endemic to the Iberian Peninsula, including gypsophytes of particular ecological, evolutionary and biochemical interest, and taxa that have undergone both sympatric and allopatric genetic differentiation. The niche shift among these taxa has been assessed using ecological niche modelling and ordination techniques, adopting a niche overlap approach to compare the similarity and equivalency of the ecological niches. We used the Maximum Entropy method to study the potential distribution of these taxa in different eras: the Last Glacial Maximum (LGM), the Mid Holocene and the current conditions. We present evidence of niche shift during the speciation of G. bermejoi, with a strong niche overlap between the parental taxa (G. struthium subsp. struthium and G. tomentosa), yet both overlap much more weakly with the hybrid species. This phenomenon may be explained by genetic and epigenetic interactions, and it has been described in other species. We also studied the sister subspecies G. struthium subsp. struthium and G. struthium subsp. hispanica, with mostly allopatric distributions and with the Iberian System mountain range acting as a geographical barrier. The Iberian System and other mountain ranges may have favored differences in the climatic conditions on either side of the mountain range, which is consistent with an incipient process of bioclimatic ecological speciation. These results seem to indicate that niche shift can occur over very different timespans. In the case of G. bermejoi, speciation may have produced significant niche shifting in one or two generations due to its alloploid nature. By contrast, G. struthium subsp. struthium and G. struthium subsp. hispanica seem to have undergone a more gradual process of allopatric genetic differentiation driven by bioclimatic factors. Both these processes are relatively recent and they will have been strongly influenced by the climate change at the end of LGM.

Citation: de Luis M, Bartolomé C, García Cardo Ó, Martínez Labarga JM, Álvarez-Jiménez J (2018) Sympatric and allopatric niche shift of endemic Gypsophila (Caryophyllaceae) taxa in the Iberian Peninsula. PLoS ONE 13(11): e0206043. https://doi.org/10.1371/journal.pone.0206043

Editor: Ulrich Melcher, Oklahoma State University, UNITED STATES

Received: March 5, 2018; Accepted: October 5, 2018; Published: November 7, 2018

Copyright: © 2018 de Luis 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 paper and its Supporting Information files.

Funding: The authors received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

1-Introduction

Gypsum outcrops in the Iberian Peninsula constitute challenging and unusual habitats for plants. Considered to be the only reservoir of these soils in Europe [1], they are ranked as priority areas for conservation by the European Union [2]. These habitats are scattered in patches, concentrated in the eastern half of the Peninsula (Fig 1A), a fragmented distribution that is not dissimilar to the biogeography of island ecosystems [1]. Although gypsum soils are challenging environments for plants, they harbor a diversity of flora that includes many endemic species. Thus, they are of particular interest to study plant evolution and ecology.

Download:

Fig 1.

(A) Map of the Iberian Peninsula showing the presence of Ononis tridentata L., a plant that is indicative of gypsum and gypsiferous loam soils. (B to E) MaxEnt maps showing the bioclimatic suitability for G. tomentosa (B), G. bermejoi (C), G. struthium subsp. struthium (D) for G. struthium subsp. hispanica (E). We have included the points where the taxon is currently present (yellow dots).

https://doi.org/10.1371/journal.pone.0206043.g001

The Gypsophila L. genus (Caryophyllaceae) has its origins in the Caucasus Mountains and the Irano-Turanian region [3–6], with its center of diversity in Turkey [7], although it now includes some Iberian endemisms. In the Iberian Peninsula this genus contains 9 taxa included in 8 species (López González, 1990), of which 5 are endemics for Spain: G. montserratii Fernández Casas, G. struthium subsp strutihum L., G. struthium subsp hispanica (Willk.) G. López, G. bermejoi G. López, G. tomentosa L. [8]. The last four can be considered as gypsophytes according to the expert criteria [9,10] (Fig 1B to 1E). The species of Gypsophila are typical of rock-dwelling habitats or in situations of little edaphic development and lithosols (G. repens L., G. montserratii, G. struthium), or alteration habitats such as roadsides, disturbed land and farmlands (G. bermejoi, G. tomentosa, G. elegans MB, G. muralis L. and G. pilosa Hudson); almost all species can characterize steppes.

Gypsiferous soils represent difficult environments for plants, most remarkably for their strong xericity, the presence of a crusty surface and serious nutritional imbalances [11]. Gypsophytes are of interest in biochemical terms due to their tendency to accumulate certain minerals and their ability to produce specific secondary metabolites. As such, the production of antioxidants, like phenols and flavonoids, and that of saponins has been studied in Gypsophila [12–14]. Moreover, the singular ecological conditions of these soils has produced plants highly adapted to their environment, with an abundance of endemic species. This circumstance, along with the fragmentation of their habitats, makes these species a suitable model to study plant evolution and speciation [15].

While the origin of the genus has been established in the Neogene period, c.a. 5.7 Million years ago (Mya: [16]), it remains unclear when gypsophytes became established in the Iberian Peninsula. Given that the Messinian Salinity Crisis [17,18] ended at the start of the Pliocene, it is possible that these plants could have arrived on the Iberian Peninsula at that time and had their current distributions affected by Quaternary climate changes [19]. We set out to assess the role of these climatic oscillations in the speciation and niche shift of the Iberian Gypsophila endemisms, as well as the timespan of these effects. Indeed, these taxa offer instances of both sympatric and allopatric genetic differentiation.

In terms of the Iberian Gypsophila species, here we have studied two subspecies of Gypsophila struthium L. that are mostly found in allopatric ranges [20]. In terms of their distribution, G. struthium subsp. hispanica is mainly found in the northeastern quadrant of the Iberian Peninsula, whereas G. struthium subsp. struthium occupies the southeast quadrant. Both zones are separated by the Iberian System mountain range. Some studies have been carried out into the structure and genetic diversity of these two subspecies [21], revealing weak but significant genetic differentiation between them, possibly due to a more recent diversification in the Pliocene (5.3–2.6 Mya) and Pleistocene (2 Mya-10,000 years ago) epochs [22]. In this interval of approximately 5.3 Mya to about 10,000 years ago, the climate is known to have undergone notable changes that have had a decisive influence on the genetic structure of populations of different organisms [21].

Species Distribution Models show that these climatic oscillations have forced significant changes in the range of these taxa [23]. These changes, along with the existence of the Iberian System mountain range, which serves as a boundary between the distribution zones of G. struthium subsp. struthium and G. struthium subsp. hispanica (Fig 1D and 1E), may have had an important role in favoring different climatic conditions between the ranges of both taxa. Indeed, these climatic changes may perhaps have been as important as the physical barrier that blocked the genetic flow between both subspecies, since a zone of contact does exist between them. Bayesian analysis reveals populations with a mixture of ancestral gene clusters where both subspecies overlap [22]. Both these characteristics indicate that the reproductive barrier existing between these subspecies is incomplete, which we consider to be similar to cases of allopatric speciation that may be currently in progress. The fact that the differences in the bioclimatic conditions on both sides of the Iberian System seem to have influenced the genetic differentiation between both subspecies would make this situation similar to a case of ecological speciation. Ecological speciation can be defined as the emergence of barriers between populations due to divergent selection based on ecological factors. That is, natural selection would arise as a consequence of the interaction of organisms with their environment or with other organisms [24]. According to our data, climate seems to have played a key role in this divergent selection. However, the influence of other factors cannot be ruled out, such as biotic factors, the interaction of biotic and climatic factors, or phenomena such as genetic drift or a founder effect.

We have also considered a tetraploid allopolyploid gypsophyte from an ecological point of view, Gypsophila bermejoi G. López [25]. Its parental species are G. struthium subsp. struthium [25] and G. tomentosa [25]. Polyploidy is characterized by the presence of two or more sets of paired or homologous chromosomes in each nucleus, in this case both sets of chromosomes proceeding from different species (Allopolyploidy). This phenomenon is responsible for the appearance of new species and it is a crucial event in the diversification of species, particularly in plants [26]. This process requires a few generations to become established and we wanted to determine if it may be associated with an ecological niche shift. In general, one parental genome is preferentially expressed over the other in both natural and synthetic allopolyploids [27]. In these species, new phenotypes may arise through genetic and epigenetic phenomena, and they generally occupy environments that differ from those occupied by their progenitors. Furthermore, the polyploid hybrids that form may express extreme traits [28–32]. Thus, it makes sense to think that this phenomenon will affect the ecological niche of the hybrid species.

Species Distribution Models have been employed successfully to study a wide range of ecological situations [33–36]. These tools can help understand the effect of quaternary climatic oscillations and the possible changes in the range of species over time. Such models could highlight whether climate change had a significant influence on the speciation process that gave rise to G. bermejoi [23], and on the genetic differentiation between the other G. struthium subspecies. Accordingly, we have used ecological niche tests to assess the possible niche shift in these taxa. The data obtained point to a central role of bioclimatic changes on the evolution of Gypsophila in the Iberian Peninsula.

2-Materials and methods

2.1-Study area and species

The area studied here includes the gypsum steppes of the Iberian Peninsula, a territory with an approximate extent of 623,000 km² located between latitudes 36°00’08” N—43°47’38” N and longitudes 9°29’00” O—3°19’00” E. The gypsum outcrops in this territory cover a total extension of 32,487 km² (6.1% of the Peninsula) [1], and they are concentrated in the eastern half of the Peninsula under the influence of a Mediterranean climate.

In this study, we focused on the genetic differentiation of distinct taxa of Gypsophila (Caryophyllaceae): Gypsophila bermejoi (2n = 68), an allopolyploid species found on verges and slopes in areas of gypsum soil; its parental species, G. struthium subsp. struthium (2n = 34) and G. tomentosa (2n = 34); and G. struthium subsp. hispanica (2n = 34), a sibling taxon of G. struthium subsp. struthium. All these perennial plants are endemic to the Iberian Peninsula, inhabiting salt-rich substrates and fundamentally, gypsum soils.

2.2-Data sources

Two types of data are required for the modeling of ecological niches using MaxEnt and for niche comparisons: species occurrence data and a set of environmental data for those locations. Here, we used species occurrence data from the Global Biodiversity Information Facility (GBIF) database [37]. These data were carefully filtered. For instance, we detected some wrong citations of G. struthium subsp. hispanica in the range of G. struthium subsp. struthium. In terms of the environmental variables, we used the bioclimatic variables from The WorldClim portal (www.worldclim.org) that makes publically available data for 19 bioclimatic variables [38]. These data are presented as a set of world maps for the different bioclimatic variables, which are the extrapolated output of values taken from meteorological stations distributed around the world. In this same platform, past and future maps of these bioclimatic variables can also be found, generated using different climate models. In this study we also used the bioclimatic maps for the mid-Holocene and the Last Glacial Maximum (LGM), generated by the Community Climate System Model (CCSM4). This model unifies four separate models of the atmosphere, land, oceans and sea-ice, generating a simulation of the global climate [39]. In this study, we only used selected bioclimatic variables according to the ecological profile of the species studied and the climatic limiting factors of the area (Table 1). Moreover, as we only considered variables with r <0.95 [40], the number of localities for some species is relatively low due to the endemic nature of the taxa. The number of variables selected, seven in this case, must be lower than 10 x the number of species occurrences in order to prevent over-parameterization in the niche modeling techniques used [41,42].

Download:

Table 1. List of the environmental variables selected to implement both the MaxEnt species distribution models and the models for niche comparison.

https://doi.org/10.1371/journal.pone.0206043.t001

2.3-Maximum Entropy (MaxEnt) Model

To model ecological niches and areas of potential distribution, we used the Maximum Entropy (MaxEnt) approach [43,44]. The algorithms required are currently implemented in R language and using a graphic interface (freely available at http://biodiversityinformatics.amnh.org/open_source/maxent/). For this work the most recent version of the program available was used (MaxEnt 3.4.1: for an explication of the method, see [43–47]). Basically, this tool assesses the probability of the presence of the species in function of the environmental variables selected. The inputs are data files on the presence of the species and a series of maps of the environmental variables considered to be significant for initial values that can be interpreted as an index of suitability of the habitat for that particular species [43]. We dealt with the autocorrelation issues by eliminating the redundant presence in each pixel on the scale of the bioclimatic variables used. We used 70% of the presence records to train the models and 30% to test them.

Two statistics were used to assess the models’ predictive performances: the Area Under the Curve (AUC) and True Skill Statistics (TSS). For the AUC approach, we have to plot the Receiver Operating Characteristic (ROC) curve. This curve represents sensitivity (True Positive Rate) vs. 1- specificity (True Negative Rate) at various threshold values. Or in other words, this curve is the true positive rate as a function of the false positive rate. Thus, If we obtain a diagonal line our model is uninformative (not better than random guessing). Increasing area under the ROC curve implies better model fit [43]. TSS takes into account both omission and commission errors, and success as a result of random guessing. It does express the hit rate relative to the false positive rate. TSS values ranges from -1 to +1 (perfect agreement). Values of zero or less indicate a performance no better than random [48].

This study focused on the effect of climatic oscillations and as such, we used bioclimatic variables to generate the models. Given the strict gypsophilic nature of these plants, the real suitability is 0 in all the locations without gypsum soils. To trace the areas with gypsum soils we chose to use records of the presence of a gypsum indicator plant, Ononis tridentata L. [10,11]. Then we obtained the bioclimatic suitability values only for those points, for the case of G. bermejoi and its parental species. For G. struthium subsp. struthium and G. struthium subsp. hispanica, these suitability values were taken at the current presence points of the taxon and those of its sister subspecies. All these taxa are confined to gypsum soils but, in the second case, our goal was to asses the suitability of each subspecies in its sister’s range.

In choosing the functions “feature”, we deactivated the functions hinge and threshold. In this way, the response curves obtained were easier to interpret and they were better adjusted to the ecological theory of the niches [47].

2.4-Niche comparison

The different niches of the Gypsophila taxa were compared using the method developed by Broennimann et al. (2012) [48,49], an approach used successfully in a wide range of plant, animal and virus case studies [50–56]. The method adopts an ordination approach to assess the occurrence density along two environmental axes. The bioclimatic variables included are reduced using a Principal Component Analysis (PCA) correlation matrix [57] and the environmental space is defined by the first two axes of the PCA, which is limited by the minimum and maximum environmental values across the whole study area. The environmental space is divided into a grid of r x r cells, where each cell corresponds to a unique combination of environmental conditions. The species occurrences are plotted onto this environmental space grid and a kernel smoothing method is then applied to them. We have plotted the niches of the species in pairs to make their comparison easier [58].

Niche overlap is calculated using Schoener’s D metric [59], a metric that ranges from 0 (no overlap) to 1 (complete overlap) [60]. In this approach, an unbiased estimate of D is calculated using a kernel density function that is applied to the occurrence densities. Statistical significant niche overlaps are then determined using niche similarity and niche equivalency tests [49,60], the latter determining whether the niches of two taxa are equivalent in two ranges. In other words, whether the niche overlap is constant when randomly redistributing the occurrences of both taxa among the two geographical areas. All these occurrences are pooled and randomly relocated into two datasets, maintaining the number of occurrences in the original datasets. This was repeated 100 times to generate a null distribution that could be compared with the D metric observed. It is important to note that non-significant results only mean that the niches are not identical, not that they are dissimilar. The niche similarity test determines whether the overlap between niches in two ranges is different from the overlap between the observed niche in one range and niches selected at random from the other range. The random niches are generated by randomly shifting the centroid of the second taxon in the environmental space. Again, the process is repeated 100 times to generate a null distribution. Niche similarity tells us if one taxon’s niche is better at predicting the second groups niche than randomly generated niches from the background area.

3-Results

From the models generated with MaxEnt for the three studied species, the AUC values obtained were 0.965 (G. bermejoi), 0.934 (G. tomentosa), 0.933 (G. struthium struthium) and 0.936 (G. struthium hispanica), all of which were sufficiently high to accept these models. The TSS values for the same species were 0.833 (G. bermejoi), 0.686 (G. tomentosa), 0.621 (G. struthium struthium) and 0.691 (G. struthium hispanica), with values above 0.6 considered to be good and 0.2–0.6 to be fair to moderate.

3.1-Range changes in Gypsophila since Last Glacial Maximum (LGM)

The climatic oscillations during the Quaternary may have had an important influence on the evolution of the taxa studied. To assess the possible range changes, we used MaxEnt to project these models onto the climatic conditions calculated for the Last Glacial Maximum (LGM), the Mid-Holocene period (MH) and the present. The maps we obtained showed important changes in the potential distribution of G. struthium subsp. struthium and G. struthium subsp. hispanica.

For G. struthium subsp. hispanica the maximum suitability areas during the LGM are not far from its current distribution. These areas lie south of the eastern Pyrenees, in the Ebro valley and in a region close to the eastern coast line of the Iberian Peninsula. The current distribution for this taxon is shifted slightly towards the west, to areas where there are patches of gypsum soils that make it possible that this taxon existed there during the LGM. Nevertheless, the values of climatic suitability in gypsum soil areas are very low (Fig 2A).

Download:

Fig 2. Habitat suitability predicted by the MaxEnt models for G. struthium subsp. hispanica.

Habitat suitability map for the Last Glacial Maximum (A), the Mid-Holocene period (B) and in the current climatic conditions (C). (D) Habitat suitability values (R software standard boxplot) in the Last Glacial Maximum, the Mid-Holocene and in the current climatic conditions measured at the points where the taxon is currently present. In (E) we show a similar plot but the values of suitability for G. struthium subsp. hispanica are taken at the current locations of its sister subspecies, G. struthium subsp. struthium. (F) Current distribution of G. struthium subsp. struthium (brown dots) and G. struthium subsp. hispanica (light green dots) over the Glacial Maximum suitability map for G. s. hispanica (values > 0.25). Imagery: PNOA 2018 CC-BY 4.0 ign.es.

https://doi.org/10.1371/journal.pone.0206043.g002

By contrast, the climatic suitability for G. struthium subsp. struthium during the LGM appeared to be strong in the Ebro valley and in the eastern coastal region. These areas overlap with the maximum suitability in that period for G. struthium subsp. hispanica but the suitability for G. struthium subsp. struthium at those areas seemed to be much higher (Fig 3A and 3E).

Download:

Fig 3. Habitat suitability predicted by the MaxEnt models for G. struthium subsp. struthium.

Habitat suitability map for the Last Glacial Maximum (A), the Mid-Holocene period (B) and in the current climatic conditions (C). (D) Habitat suitability values (R software standard boxplot) in the Last Glacial Maximum, the Mid-Holocene and in the current climatic conditions measured at the points where the taxon is currently present. In (E) we show a similar plot but the values of suitability for G. struthium subsp. struthium are taken at the current locations of its sister subspecies, G. struthium subsp. hispanica. (F) Current distribution of G. struthium subsp. struthium (brown dots) and G. struthium subsp. hispanica (light green dots) over the Glacial Maximum suitability map for G. s. struthium (values > 0.25). Imagery: PNOA 2018 CC-BY 4.0 ign.es.

https://doi.org/10.1371/journal.pone.0206043.g003

We also obtained the suitability values from the MaxEnt models at the current locations for both subspecies during the LGM, the Mid-Holocene period and in the current climatic conditions. As expected, the suitability values predicted by the model of G. struthium subsp. hispanica at its current location increase over time (Fig 2D). Moreover, the suitability values for this subspecies at the present points of G. struthium subsp. struthium never reach high values. As a general rule, yet with some exceptions (see outliers in Fig 2E), G. struthium subsp. hispanica never performed very well in the current range of G. struthium subsp. struthium. By contrast, the maps for G. struthium subsp. struthium reflected a quite different behavior, whereby the suitability of this subspecies measured at its current sites increased gradually from the LGM (Fig 3). We observed a different trend for the values measured in present conditions for the sister subspecies. At the current sites of G. struthium subsp. hispanica, the G. struthium subsp. struthium was well suited in the LGM and it seems to have been very comfortable in the Ebro valley, currently an important domain in the range of G. struthium subsp. hispanica. Thus, the climatic transition to the Mid Holocene would appear to have turned this region into a much less favorable area for G. struthium subsp. struthium.

To study the case of G. bermejoi we generated maps for the bioclimatic suitability values taken only in locations with favorable soils for this species and its parental taxa (Fig 4). Again, the models show meaningful changes in the potential distribution of G. bermejoi, G. struthium subsp. struthium and G. tomentosa. (Fig 2).

Download:

Fig 4. Habitat suitability predicted by the MaxEnt models for G. bermejoi and its parents for the locations with suitable soils.

Due to the gypsophilic character of these species the real suitability is zero in soils other than gypsum and gypsiferous loam soils. Habitat suitability map for G. bermejoi during the Last Glacial Maximum (A) (notice the different coast lines for this period), the Mid-Holocene period (B) and in the current climatic conditions (C). (D) Habitat suitability values (R software standard boxplot) in the Last Glacial Maximum, the Mid-Holocene and in the current climatic conditions measured at the locations with gypsum soils. Notice that A and the first plot in D show an extremely low suitability for G. bermejoi during the LGM. It is very likely that the speciation event was effective only after the end of LGM. The panels series E to H and I to L, show similar information relative to G. struthium subsp. struthium and G. tomentosa (parental species of G. bermejoi) respectively. The parental species show a high degree of sympatry during the LGM and probably they could interbreed. Even though, it is likely that the climatic conditions were preventing the hybrid G. bermejoi to thrive during that climatic period.

https://doi.org/10.1371/journal.pone.0206043.g004

During the LGM both, G. struthium subsp. struthium and G. tomentosa seemed to take shelter on the eastern and south eastern coastal strip of the Iberian Peninsula, with this zone extending into inland locations along the Ebro Valley (Fig 4E and 4I). They show a high degree of sympatry. In contrast, the suitability for G. bermejoi is almost zero during this period (Fig 4A). This can be seen more precisely in the box plots (Fig 4D, 4H and 4L).

This situation changes remarkably during the Mid Holocene. In most of the gypsum outcrops, bioclimatic suitability decreases for G. struthium subsp. struthium and G. tomentosa. But in the case of G. bermejoi this climatic transition seems to favor its presence in many locations of the Iberian Peninsula. The bioclimatic suitability values for this species increases markedly for this period.

The current climatic conditions, again, favor higher bioclimatic suitability values in most of the favorable locations for the parental taxa (Fig 4G and 4K). The evolution of these values through can be clearly seen in Fig 4H and 4L. G. bermejoi shows a very different behavior. For the current climatic conditions its bioclimatic suitability decreases. But now, the box plots show a relatively high number of outliers (Fig 4D). These values correspond to the limited number locations where this plant feels comfortable, as expected in an endemic species.

3.2-Comparison of ecological niches

We compared the niches of these taxa using niche equivalence and niche similarity tests (Table 2). In the case of the sympatric speciation of G. bermejoi, we compared its ecological niche to those of its parental species, G. struthium subsp. struthium and G. tomentosa. In the first case the results show that the ecological niches are neither equivalent nor similar. In the second one, there could be some degree of niche similarity but not equivalency. The values of Schoener’s D between the parental species (G. struthium subsp. struthium and G. tomentosa) are relatively high and this is of no surprise given that the plants must coincide to some degree to be able to interbreed. Interestingly, the values of niche overlap are much lower when these parental species are compared to the hybrid species G. bermejoi. These data, along with the PCA (Fig 5) plots favors the existence of niche shift during the formation of G. bermejoi.

Download:

Fig 5. PCA plots for the Gypsophila taxa studied.

The environmental space is defined by the first two axes of the PCA analysis and it is limited by the minimum and maximum environmental values across the whole study area. Contour lines draw suitability values [58]. The different taxa have been plotted in pairs to make comparisons easier: (A) G. bermejoi (red) vs. G. struthium subs. struthium (blue), (B) G. bermejoi (red) vs. G tomentosa (blue), (C) G. struthium subs. struthium (red) vs. G. tomentosa (blue), (D) G. struthium subs. struthium (red) vs. G struthium subsp. hispanica (blue).

https://doi.org/10.1371/journal.pone.0206043.g005

Download:

Table 2. Schoener’s D and niche similarity tests for Iberian Gypsophila taxa.

The first number in the cells corresponds to the observed value of Schoener’s D. The not significant P-values are indicated by “ns”.

https://doi.org/10.1371/journal.pone.0206043.t002

The PCA plots for G. bermejoi and its two parental species showed remarkable differences between the niches (Fig 5A and 5B), with G. bermejoi revealing itself to be a species with an ecological niche much narrower than those of G. struthium subsp. struthium and G. tomentosa.

For the sister allopatric subspecies of G. struthium, the results again showed that the niches are neither equivalent nor similar. Despite they being considered subspecies, the Schoener’s D value was comparable to those obtained between different species of this genus (Table 2). Moreover, the PCA plot again showed clear differences for the climatic niches of both taxa, with G struthium subsp. hispanica displaying a narrower ecological niche than G. struthium subsp. struthium.

4-Discussion

In this study, we have examined the evolution of several Gypsophila species endemic to the Iberian Peninsula, using similarity and equivalence tests to demonstrate evidence of niche shift in these species. The ecological niche of G. bermejoi is neither equivalent nor similar to that of its parental species, and a similar situation arises when the niches of the sister subspecies of G. struthium are compared [25].

The ecological niche of G. bermejoi has lower Schoener’s D values relative to both parental species, although higher values were obtained when comparing the niches of the parental species (G. struthium subsp. struthium and G. tomentosa). Indeed, the hybrid species that was derived from these parental types has neither an equivalent nor a similar niche. It is not uncommon for allopolyploid species to express extreme phenotypes and the phenotypic traits related to the ecological behavior of these species are no exception. Such a phenomenon would explain sudden ecological niche shift in one or two generations, a very short time span in evolutionary terms. A number of research works point to rapid epigenetic changes in allopolyploids genesis, under both synthetic and natural conditions [31]. According to Rieseberg [30], large and rapid adaptive transitions can be explained by hybridization because “unlike mutation, it provides genetic variation at hundreds or thousands of genes in a single generation” (emphasis ours). Differences in gene expression have been observed between the diploid parental species and a synthetic F1 hybrid. According to Ainouche and Wendell [28] these results “showed that a significant fraction of expression bias found in allotetraploids likely is initiated by genome merger per se” (emphasis ours). We aim to demonstrate that the timespan for niche shift can vary widely. We think that speciation by hybridization could be in the fastest extreme of the timespan range.

There is evidence that climate is a crucial driving force in this event and Species Distribution Models indicate a sympatric distribution of the parental species during the LGM. The eastern coastal region was a refuge for both taxa, permitting the cross pollination between two species as occurred recently to produce the hybrid Gypsophila x castellana Pau [25]. However, environmental conditions prevented the hybrid from thriving due to its narrow bioclimatic niche and as such, climate would have repressed the speciation process throughout the Last Glacial period. Nevertheless, the climatic transition to the Holocene period would have triggered the formation of G. bermejoi [23].

By contrast, the formation of the G. struthium sister subspecies seems to have taken longer and it involves allopatry, although again the climate seems to be a driving factor in the genetic divergence of G. struthium subsp. struthium and G. struthium subsp. hispanica. The quaternary climatic oscillations produced critical changes in the ranges of the ancestral populations and the potential distribution of G. struthium subsp. struthium became limited to an eastern coastal strip of territory and the Ebro Valley during the LGM. The models produce high suitability values for this subspecies in these areas (Fig 3E), with a weaker habitat suitability signal for G. struthium subsp. hispanica over the same period, partially overlapping with the range of G. struthium subsp. struthium. Along with the absence of geographical barriers, this makes it difficult to accept the existence of G. struthium subsp. hispanica as a differentiated taxon during the LGM. Indeed, we favor the presence of ancestral populations similar to G. struthium subsp. struthium during this period.

The climatic change at the end of the Glacial Period enabled these populations to colonize or re-colonize the gypsum outcrops in the interior of the Iberian Peninsula. According to the MaxEnt maps, the climatic conditions during the Mid Holocene period favored the presence of G. struthium subsp. struthium in the central and south eastern regions of the Peninsula (Southwest and South of the Iberian System). Conversely, the suitability of this subspecies in the Ebro Valley (Northeast of the Iberian System) decreases abruptly. The climatic contrast between both areas was probably enhanced by the presence of the Iberian System mountain range [61,62], which makes it even more plausible that such climate changes exerted selective pressure on these populations. The outcome of this situation would be the genetic differentiation of the populations on either side of the mountains, similar to a process of ecological speciation [63–66].

We believe that most of the genetic differentiation between these subspecies occurred after the LGM. The models seem to point to the “in situ” substitution of G. struthium subsp. struthium by G. struthium subsp. hispanica in the Ebro Valley, and that climate was an important driving factor in this process. We favor a process similar to ecological speciation, in which the ancestral populations (similar to those of G. struthium subsp. struthium) are gradually replaced with G. struthium subsp. hispanica in the Ebro Valley. This scenario would explain why the current locations of G. struthium subsp. hispanica match almost perfectly with a high suitability region for G. struthium subsp. struthium during the LGM.

We want to stress that the complex genetic structure of both subspecies is not easy to explain and that the influence of other factors, both biotic and abiotic, cannot be ruled out. Nonetheless, the scenario could outline the recent evolutionary history of G. struthium subsp. hispanica and G. struthium subsp. struthium.

5-Conclusions

From the results obtained, we can draw the following conclusions:

Different mechanisms for niche shift arise in the Gypsophila genus, affecting both sympatric and allopatric populations. In the former, new allopolyploid species can display a very different ecological behavior from the parental species. By contrast, in allopatric populations processes of genetic divergence may have been favored by the presence of a geographical barrier and different climatic conditions.
The timespan of these processes can vary widely. Sudden niche shift was possible in the allopolyploid species G. bermejoi, with the new hybrid species likely appearing in one or two generations. For the separation of the two subspecies of G. struthium, our results point to a more gradual process of niche shift resulting from genetic differentiation that began at the end of the Last Glacial Maximum.
It seems reasonable to discard the presence of G. bermejoi in the Iberian Peninsula during the LGM. This conclusion is supported by the fact of its very narrow bioclimatic niche (Fig 5A and 5B) Due to the sympatric distribution of its parental taxa during the LGM, we think that these taxa could have been interbreeding during that period, but the climatic conditions were repressing the speciation process. During the Mid Holocene the situation changes dramatically (Fig 4A and 4B) and now it is possible for the hybrid taxon (G. bermejoi) to thrive. We think that the effective formation of populations of G. bermejoi was posible only after the climatic transition between the LGM and the Mid Holocene took place [23].
We favor a more ancestral character of G. struthium subsp. struthium. During the LGM, G. struthium subsp. struthium did it better in the current range of G. struthium subsp hispanica. Even better than in its current range (Fig 3D and 3E). During the same period, the situation is very different for G. struthium subsp. hispanica. Its suitability is almost 0 in the range of G. struthium subsp. struthium and poor in its own current range. This makes more difficult to accept the presence of G. struthium subsp. hispanica as a separated taxon in the Iberian Peninsula during this period (LGM). In others words: during the LGM G. struthium subsp. struthium seemed to feel at home in the locations where we now find the G. struthium subsp. hispanica. That is why we think that the ancestral populations of G. struthium subsp. hispanica in the Ebro Valley were more similar to the current G. struthium subsp. struthium and that they gradually evolved in situ to G. struthium subsp. hispanica.
The quaternary climatic oscillations played a crucial role in this divergence and we believe it is impossible to disentangle the evolutionary history of these taxa without taking into account the quaternary climatic oscillations that occurred in the last 25,000 years.
Despite the differences in mechanisms and timespan, several niche shift events in Iberian endemic Gypsophila taxa are relatively recent and they do not predate the LGM.

Supporting information

S1 Table. Habitat suitability predicted by the MaxEnt models for G. struthium subsp. hispanica, during the Last Glacial Maximum, the Mid-Holocene and in the current climatic conditions measured at the points where the taxon is currently present.

https://doi.org/10.1371/journal.pone.0206043.s001

(CSV)

S2 Table. As S1 but the values of suitability for G. struthium subsp. hispanica are taken at the current locations of its sister subspecies, G. struthium subsp. struthium.

https://doi.org/10.1371/journal.pone.0206043.s002

(CSV)

S3 Table. Habitat suitability predicted by the MaxEnt models for G. struthium subsp. struthium, during the Last Glacial Maximum, the Mid-Holocene and in the current climatic conditions measured at the points where the taxon is currently present.

https://doi.org/10.1371/journal.pone.0206043.s003

(CSV)

S4 Table. As S3 but the values of suitability for G. struthium subsp. struthium are taken at the current locations of its sister subspecies, G. struthium subsp. hispanica.

https://doi.org/10.1371/journal.pone.0206043.s004

(CSV)

S1 Fig. Niche similarity test histograms.

https://doi.org/10.1371/journal.pone.0206043.s005

(TIF)

S2 Fig. Niche equivalency test histograms.

https://doi.org/10.1371/journal.pone.0206043.s006

(TIF)

Acknowledgments

We thank D. Blas M. Benito from the Environmental and Ecological Change Research Group (University of Bergen) for his suggestions for the development of our research.

References

1. Mota JF, Sánchez-Gómez P, Guirado JS. Diversidad vegetal de las yeseras ibéricas. El reto de los archipiélagos edáficos para la biología de la conservación. ADIF-Mediterráneo Asesores Consultores, Almería. 2011.
2. Habitats Directive 92/43/EEC, habitat 1520.
3. Barkoudah YI. A revision of Gypsophilla, Bolanthus, Ankyropetalum and Phryna. 1962; 9(S3): 1–203.
- View Article
- Google Scholar
4. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, et al. Global vegetation change through the Miocene/Pliocene boundary. Nature. 1997; 389: 153–158.
- View Article
- Google Scholar
5. Ramstein G, Fluteau F, Besse J, Joussaume S. Effect of orogeny, plate motion and land sea distribution on Eurasian climate change over the past 30 million years. Nature. 1999; 386: 788–795.
- View Article
- Google Scholar
6. Costa-Tenorio M, Morla-Juaristi C, Sainz-Ollero H. Los bosques ibéricos. Barcelona: Planeta. 1998.
7. Korkmaz M, Dogan NY. Biogeographic pattern of genetic diversity detected by RAPD and ISSR analysis in Gypsophila (Caryophyllaceae) species from Turkey. Genetics and Molecular Research. 2015; vol. 14, no 3, p. 8829–8838. pmid:26345814
- View Article
- PubMed/NCBI
- Google Scholar
8. Martínez-Labarga JM. (2014). Estudios corológicos de plantas vasculares en la cuenca media del Tajo (Doctoral dissertation, Montes).
9. Mota JF, Gómez PS, Calvente MEM, Rodríguez PC, Lumbreras EL, De la Cruz Rot M, et al. (2009). Aproximación a la checklist de los gipsófitos ibéricos. In Anales de Biología (No. 31, pp. 71–80).
- View Article
- Google Scholar
10. Mota Poveda JF, Garrido Becerra JA, Pérez-García FJ, Salmerón-Sánchez E, Sánchez-Gómez P, Merlo E. Conceptual baseline for a global checklist of gypsophytes. Lazaroa. 2016; 37: 7–30.
- View Article
- Google Scholar
11. Escudero A, Palacio S, Maestre FT, Luzuriaga AL. (2015). Plant life on gypsum: a review of its multiple facets. Biological Reviews, 90(1), 1–18. pmid:25756149
- View Article
- PubMed/NCBI
- Google Scholar
12. Acebes B, Bernabé M, Diaz-Lanza AM, Bartolomé C. Two new sulfated saponins from the roots of Gypsophila bermejoi. J Nat Prod. 1998; 61(12): 1557–1559. pmid:9868165
- View Article
- PubMed/NCBI
- Google Scholar
13. Acebes B, Daz-Lanza AM, Bernabé M. A saponin from the roots of Gypsophila bermejoi. Phytochemistry. 1998; 49(7): 2077–2079. pmid:9883593
- View Article
- PubMed/NCBI
- Google Scholar
14. Boscaiu M, Sánchez M, Bautista I, Donat P, Lidón A, Llinares J, et al. Phenolic compounds as stress markers in plants from gypsum habitats. Bull Univ Agric Sci Vet Med Cluj Napoca, Horticulture. 2010; 67(1): 1843–5254.
- View Article
- Google Scholar
15. Escudero A, Palacio S, Maestre FT, Luzuriaga AL, et al. Plant life on gypsum: a review of its multiple facets. Biological Reviews. 2015; vol. 90, no 1, p. 1–18. pmid:25756149
- View Article
- PubMed/NCBI
- Google Scholar
16. Frajman B, Eggens F, Oxelman B. Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae): a multigene phylogenetic approach with relative dating. Systematic Biology. 2009; 58: 328–345. pmid:20525587
- View Article
- PubMed/NCBI
- Google Scholar
17. Hsü KJ, Montadert L, Bernoulli D, Biancacita M, Erickson A, Garrison RE, et al. History of Mediterranean salinity crisis. Nature. 1977; 267:399–403.
- View Article
- Google Scholar
18. Bocquet G, Wilder B, Kiefer H. The Messinian model: a new outlook for the floristics and systematics of the Mediterranean area. Candollea.1978; 33: 269–287.
- View Article
- Google Scholar
19. Willis KJ, Niklas KJ. The role of Quaternary environmental change in plant macroevolution: the exception or the rule? Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2004; vol. 359, no 1442, p. 159–172. pmid:15101573
- View Article
- PubMed/NCBI
- Google Scholar
20. G.tomentosa: GBIF.org (10th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.my22ws. G. struthium subs. struthium:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.dzjhbc. G. bermejoi:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.engt9m.
21. Hewitt GM. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society.1996; 58: 247–276.
- View Article
- Google Scholar
22. Martínez-Nieto MI, Segarra-Moragues JG, Merlo E, Martínez-Hernández F, Mota JF. Genetic diversity, genetic structure and phylogeography of the Iberian endemic Gypsophila struthium (Caryophyllaceae) as revealed by AFLP and plastid DNA sequences: connecting habitat fragmentation and diversification. Botanical Journal of the Linnean Society. 2013; vol. 173, no 4, p. 654–675.
- View Article
- Google Scholar
23. de Luis M, Bartolomé C, García Cardo Ó, Álvarez-Jiménez J. Gypsophila bermejoi G. López: A possible case of speciation repressed by bioclimatic factors. PloS one. 2018; vol. 13, no 1, e0190536. pmid:29338010
- View Article
- PubMed/NCBI
- Google Scholar
24. Rundle HD, Nosil P. Ecological speciation. Ecology letters. 2005; vol. 8, no 3, p. 336–352.
- View Article
- Google Scholar
25. López G. Gypsophila bermejoi G. López, sp. nov. y algunos comentarios sobre el género Gypsophila con relación a Flora Iberica. An Jard Bot Madr.1984; 41(1): 35–38.
- View Article
- Google Scholar
26. Soltis PS, Soltis DE. The role of hybridization in plant speciation. Annu Rev Plant Biol. 2009; 60: 561–588. pmid:19575590
- View Article
- PubMed/NCBI
- Google Scholar
27. Feldman M, Levy AA, Fahima T & Korol A. Genomic asymmetry in allopolyploid plants: wheat as a model. Journal of experimental botany, 2012, vol. 63, no 14, p. 5045–5059. pmid:22859676
- View Article
- PubMed/NCBI
- Google Scholar
28. Ainouche ML, Jonathan FW. Polyploid speciation and genome evolution: Lessons from recent allopolyploids. In: Pontarotti P, editor. Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life. Springer International Publishing. 2014; pp. 87–113.
29. Mallet J. Hybrid speciation. Nature. 2007; 446(7133): 279. pmid:17361174
- View Article
- PubMed/NCBI
- Google Scholar
30. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, et al. (2003). Major ecological transitions in wild sunflowers facilitated by hybridization. Science, 301(5637), 1211–1216 pmid:12907807
- View Article
- PubMed/NCBI
- Google Scholar
31. Liu B, Wendel JF. Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol. 2003; 29(3): 365–379. pmid:14615180
- View Article
- PubMed/NCBI
- Google Scholar
32. Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet,2005; 6(11): 836–846. pmid:16304599
- View Article
- PubMed/NCBI
- Google Scholar
33. Bueno ML, Pennington RT, Dexter KG, Yoshino Kamino LH, Pontara V, Mesquita Neves D, et al. Effects of Quaternary climatic fluctuations on the distribution of Neotropical savanna tree species. Ecography. 2017; vol. 40, no 3, p. 403–414.
- View Article
- Google Scholar
34. Bosso L, Luchi N, Maresi G, Cristinzio G, Smeraldo S, Russo D. Predicting current and future disease outbreaks of Diplodia sapinea shoot blight in Italy: species distribution models as a tool for forest management planning. Forest Ecology and Management. 2017; vol. 400, p. 655–664.
- View Article
- Google Scholar
35. Kaki E, Gilbert F. Using species distribution models to assess the importance of Egypt's protected areas for the conservation of medicinal plants. Journal of Arid Environments. 2016; vol. 135, p. 140–146.
- View Article
- Google Scholar
36. Rovzar C, Gillespie TW, Kawelo K. Landscape to site variations in species distribution models for endangered plants. Forest Ecology and Management. 2016; vol. 369, p. 20–28.
- View Article
- Google Scholar
37. G.tomentosa: GBIF.org (10th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.my22ws. G. struthium subs. struthium:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.dzjhbc. G. bermejoi:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.engt9m
38. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. International journal of climatology. 2005; vol. 25, no 15, p. 1965–1978.
- View Article
- Google Scholar
39. Gent PR. The community climate system model version 4. Journal of Climate. 2011; vol. 24, no 19, p. 4973–4991.
- View Article
- Google Scholar
40. McCormack JE, Zellmer AJ, Knowles LL. Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation?: insights from tests with niche models. Evolution. 2010; vol. 64, no 5, p. 1231–1244. pmid:19922442
- View Article
- PubMed/NCBI
- Google Scholar
41. R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.
42. Broennimann O, Di Cola V, Guisan A. Ecospat: Spatial Ecology Miscellaneous Methods. R package version 2.1.1. 2016. https://CRAN.R-project.org/package=ecospat
- View Article
- Google Scholar
43. Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distributions. Ecological modelling. 2006; vol. 190, no 3, p. 231–259.
- View Article
- Google Scholar
44. Phillips SJ, Dudík M. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography. 2008; vol. 31, no 2, p. 161–175.
- View Article
- Google Scholar
45. Ferrandis P, Herranz J M, Copete MA. Caracterización florística y edáfica de las estepas yesosas de Castilla-La Mancha. Investigación Agraria: Sistemas y Recursos Forestales. 2005; vol. 14, p. 195–216.
- View Article
- Google Scholar
46. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ. A statistical explanation of MaxEnt for ecologists. Diversity and distributions. 2011; vol. 17, no 1, p. 43–57.
- View Article
- Google Scholar
47. Merow C, Smith MJ, Silander JA. A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography. 2013; vol. 36, no 10, p. 1058–1069.
- View Article
- Google Scholar
48. Allouche O, Tsoar A, Kadmon R. (2006). Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). Journal of applied ecology, 43(6), 1223–1232.
- View Article
- Google Scholar
49. Broennimann O, Fitzpatrick M C, Pearman P B, Petitpierre B. Pellissier L, Yoccoz NG et al. Measuring ecological niche overlap from occurrence and spatial environmental data. Global ecology and biogeography. 2012; vol. 21, no 4, p. 481–497.
- View Article
- Google Scholar
50. Aguirre‐Gutiérrez J, Serna‐Chavez HM, Villalobos‐Arambula AR, Pérez de la Rosa JA, Raes N. Similar but not equivalent: ecological niche comparison across closely–related Mexican white pines. Diversity and distributions. 2015; vol. 21, no 3, p. 245–257.
- View Article
- Google Scholar
51. Wiens JJ, Ackerly DD, Allen AP, Anacker BL. Niche conservatism as an emerging principle in ecology and conservation biology. Ecology letters. 2010; vol. 13, no 10, p. 1310–1324. pmid:20649638
- View Article
- PubMed/NCBI
- Google Scholar
52. Thompson KA, Husband BC, Maherali H. Climatic niche differences between diploid and tetraploid cytotypes of Chamerion angustifolium (Onagraceae). American Journal of Botany. 2014; vol. 101, no 11, p. 1868–1875. pmid:25366852
- View Article
- PubMed/NCBI
- Google Scholar
53. Glennon KL, Ritchie ME, Segraves KA. Evidence for shared broad‐scale climatic niches of diploid and polyploid plants. Ecology Letters. 2014; vol. 17, no 5, p. 574–582. pmid:24818236
- View Article
- PubMed/NCBI
- Google Scholar
54. Hu J, Broennimann O, Guisan A, Wang B, Huang Y, Jiang J. Niche conservatism in Gynandropaa frogs on the southeastern Qinghai-Tibetan Plateau. Scientific reports. 2016; vol. 6, p. 32624. pmid:27601098
- View Article
- PubMed/NCBI
- Google Scholar
55. Pearman PB, Guisan A, Broennimann O, Randin CF. Niche dynamics in space and time. Trends in Ecology & Evolution. 2008; vol. 23, no 3, p. 149–158.
- View Article
- Google Scholar
56. Guisan A, Petitpierre B, Broennimann O, Daehler C, Kueffer C. Unifying niche shift studies: insights from biological invasions. Trends in ecology & evolution. 2014; vol. 29, no 5, p. 260–269.
- View Article
- Google Scholar
57. Janžekovič F, Novak T. PCA–a powerful method for analyze ecological niches. En Principal component analysis-multidisciplinary applications. InTech. 2012.
58. Fernández-López J. 2017. NiceOverPlot, or when the number of dimensions does matter(R script).URL https://allthiswasfield.blogspot.com.es/2017/05/niceoverplot-or-when-number-of.html.
59. Schoener TW. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology. 1970; vol. 51, no 3, p. 408–418.
- View Article
- Google Scholar
60. Warren DL, Glor RE, Turelli M. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution. 2008; vol. 62, no 11, p. 2868–2883. pmid:18752605
- View Article
- PubMed/NCBI
- Google Scholar
61. García de Pedraza L. Fenómenos de estancamiento y Foehn. repositorio.aemet.es. 1972.
- View Article
- Google Scholar
62. Capel Molina JJ. Factores del clima de la Península Ibérica. Paralelo 37.1978; no 2, p. 5–13.
- View Article
- Google Scholar
63. Wiens JJ. Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution. 2004; vol. 58, no 1, p. 193–197. pmid:15058732
- View Article
- PubMed/NCBI
- Google Scholar
64. Rieseberg LH, Willis JH. Plant speciation. Science. 2007; vol. 317, no 5840, p. 910–914. pmid:17702935
- View Article
- PubMed/NCBI
- Google Scholar
65. Ehrlich PR, Raven PH. Differentiation of populations. Science. 1969; p. 1228–1232.
- View Article
- Google Scholar
66. Rundle HD, Nosil P. Ecological speciation. Ecology letters. 2005; vol. 8, no 3, p. 336–352.
- View Article
- Google Scholar

[ref1] 1. Mota JF, Sánchez-Gómez P, Guirado JS. Diversidad vegetal de las yeseras ibéricas. El reto de los archipiélagos edáficos para la biología de la conservación. ADIF-Mediterráneo Asesores Consultores, Almería. 2011.

[ref2] 2. Habitats Directive 92/43/EEC, habitat 1520.

[ref3] 3. Barkoudah YI. A revision of Gypsophilla, Bolanthus, Ankyropetalum and Phryna. 1962; 9(S3): 1–203.
View Article
Google Scholar

[4] View Article

[5] Google Scholar

[ref4] 4. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, et al. Global vegetation change through the Miocene/Pliocene boundary. Nature. 1997; 389: 153–158.
View Article
Google Scholar

[7] View Article

[8] Google Scholar

[ref5] 5. Ramstein G, Fluteau F, Besse J, Joussaume S. Effect of orogeny, plate motion and land sea distribution on Eurasian climate change over the past 30 million years. Nature. 1999; 386: 788–795.
View Article
Google Scholar

[10] View Article

[11] Google Scholar

[ref6] 6. Costa-Tenorio M, Morla-Juaristi C, Sainz-Ollero H. Los bosques ibéricos. Barcelona: Planeta. 1998.

[ref7] 7. Korkmaz M, Dogan NY. Biogeographic pattern of genetic diversity detected by RAPD and ISSR analysis in Gypsophila (Caryophyllaceae) species from Turkey. Genetics and Molecular Research. 2015; vol. 14, no 3, p. 8829–8838. pmid:26345814
View Article
PubMed/NCBI
Google Scholar

[14] View Article

[15] PubMed/NCBI

[16] Google Scholar

[ref8] 8. Martínez-Labarga JM. (2014). Estudios corológicos de plantas vasculares en la cuenca media del Tajo (Doctoral dissertation, Montes).

[ref9] 9. Mota JF, Gómez PS, Calvente MEM, Rodríguez PC, Lumbreras EL, De la Cruz Rot M, et al. (2009). Aproximación a la checklist de los gipsófitos ibéricos. In Anales de Biología (No. 31, pp. 71–80).
View Article
Google Scholar

[19] View Article

[20] Google Scholar

[ref10] 10. Mota Poveda JF, Garrido Becerra JA, Pérez-García FJ, Salmerón-Sánchez E, Sánchez-Gómez P, Merlo E. Conceptual baseline for a global checklist of gypsophytes. Lazaroa. 2016; 37: 7–30.
View Article
Google Scholar

[22] View Article

[23] Google Scholar

[ref11] 11. Escudero A, Palacio S, Maestre FT, Luzuriaga AL. (2015). Plant life on gypsum: a review of its multiple facets. Biological Reviews, 90(1), 1–18. pmid:25756149
View Article
PubMed/NCBI
Google Scholar

[25] View Article

[26] PubMed/NCBI

[27] Google Scholar

[ref12] 12. Acebes B, Bernabé M, Diaz-Lanza AM, Bartolomé C. Two new sulfated saponins from the roots of Gypsophila bermejoi. J Nat Prod. 1998; 61(12): 1557–1559. pmid:9868165
View Article
PubMed/NCBI
Google Scholar

[29] View Article

[30] PubMed/NCBI

[31] Google Scholar

[ref13] 13. Acebes B, Daz-Lanza AM, Bernabé M. A saponin from the roots of Gypsophila bermejoi. Phytochemistry. 1998; 49(7): 2077–2079. pmid:9883593
View Article
PubMed/NCBI
Google Scholar

[33] View Article

[34] PubMed/NCBI

[35] Google Scholar

[ref14] 14. Boscaiu M, Sánchez M, Bautista I, Donat P, Lidón A, Llinares J, et al. Phenolic compounds as stress markers in plants from gypsum habitats. Bull Univ Agric Sci Vet Med Cluj Napoca, Horticulture. 2010; 67(1): 1843–5254.
View Article
Google Scholar

[37] View Article

[38] Google Scholar

[ref15] 15. Escudero A, Palacio S, Maestre FT, Luzuriaga AL, et al. Plant life on gypsum: a review of its multiple facets. Biological Reviews. 2015; vol. 90, no 1, p. 1–18. pmid:25756149
View Article
PubMed/NCBI
Google Scholar

[40] View Article

[41] PubMed/NCBI

[42] Google Scholar

[ref16] 16. Frajman B, Eggens F, Oxelman B. Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae): a multigene phylogenetic approach with relative dating. Systematic Biology. 2009; 58: 328–345. pmid:20525587
View Article
PubMed/NCBI
Google Scholar

[44] View Article

[45] PubMed/NCBI

[46] Google Scholar

[ref17] 17. Hsü KJ, Montadert L, Bernoulli D, Biancacita M, Erickson A, Garrison RE, et al. History of Mediterranean salinity crisis. Nature. 1977; 267:399–403.
View Article
Google Scholar

[48] View Article

[49] Google Scholar

[ref18] 18. Bocquet G, Wilder B, Kiefer H. The Messinian model: a new outlook for the floristics and systematics of the Mediterranean area. Candollea.1978; 33: 269–287.
View Article
Google Scholar

[51] View Article

[52] Google Scholar

[ref19] 19. Willis KJ, Niklas KJ. The role of Quaternary environmental change in plant macroevolution: the exception or the rule? Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2004; vol. 359, no 1442, p. 159–172. pmid:15101573
View Article
PubMed/NCBI
Google Scholar

[54] View Article

[55] PubMed/NCBI

[56] Google Scholar

[ref20] 20. G.tomentosa: GBIF.org (10th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.my22ws. G. struthium subs. struthium:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.dzjhbc. G. bermejoi:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.engt9m.

[ref21] 21. Hewitt GM. Some genetic consequences of ice ages, and their role in divergence and speciation. Biological Journal of the Linnean Society.1996; 58: 247–276.
View Article
Google Scholar

[59] View Article

[60] Google Scholar

[ref22] 22. Martínez-Nieto MI, Segarra-Moragues JG, Merlo E, Martínez-Hernández F, Mota JF. Genetic diversity, genetic structure and phylogeography of the Iberian endemic Gypsophila struthium (Caryophyllaceae) as revealed by AFLP and plastid DNA sequences: connecting habitat fragmentation and diversification. Botanical Journal of the Linnean Society. 2013; vol. 173, no 4, p. 654–675.
View Article
Google Scholar

[62] View Article

[63] Google Scholar

[ref23] 23. de Luis M, Bartolomé C, García Cardo Ó, Álvarez-Jiménez J. Gypsophila bermejoi G. López: A possible case of speciation repressed by bioclimatic factors. PloS one. 2018; vol. 13, no 1, e0190536. pmid:29338010
View Article
PubMed/NCBI
Google Scholar

[65] View Article

[66] PubMed/NCBI

[67] Google Scholar

[ref24] 24. Rundle HD, Nosil P. Ecological speciation. Ecology letters. 2005; vol. 8, no 3, p. 336–352.
View Article
Google Scholar

[69] View Article

[70] Google Scholar

[ref25] 25. López G. Gypsophila bermejoi G. López, sp. nov. y algunos comentarios sobre el género Gypsophila con relación a Flora Iberica. An Jard Bot Madr.1984; 41(1): 35–38.
View Article
Google Scholar

[72] View Article

[73] Google Scholar

[ref26] 26. Soltis PS, Soltis DE. The role of hybridization in plant speciation. Annu Rev Plant Biol. 2009; 60: 561–588. pmid:19575590
View Article
PubMed/NCBI
Google Scholar

[75] View Article

[76] PubMed/NCBI

[77] Google Scholar

[ref27] 27. Feldman M, Levy AA, Fahima T & Korol A. Genomic asymmetry in allopolyploid plants: wheat as a model. Journal of experimental botany, 2012, vol. 63, no 14, p. 5045–5059. pmid:22859676
View Article
PubMed/NCBI
Google Scholar

[79] View Article

[80] PubMed/NCBI

[81] Google Scholar

[ref28] 28. Ainouche ML, Jonathan FW. Polyploid speciation and genome evolution: Lessons from recent allopolyploids. In: Pontarotti P, editor. Evolutionary Biology: Genome Evolution, Speciation, Coevolution and Origin of Life. Springer International Publishing. 2014; pp. 87–113.

[ref29] 29. Mallet J. Hybrid speciation. Nature. 2007; 446(7133): 279. pmid:17361174
View Article
PubMed/NCBI
Google Scholar

[84] View Article

[85] PubMed/NCBI

[86] Google Scholar

[ref30] 30. Rieseberg LH, Raymond O, Rosenthal DM, Lai Z, Livingstone K, Nakazato T, et al. (2003). Major ecological transitions in wild sunflowers facilitated by hybridization. Science, 301(5637), 1211–1216 pmid:12907807
View Article
PubMed/NCBI
Google Scholar

[88] View Article

[89] PubMed/NCBI

[90] Google Scholar

[ref31] 31. Liu B, Wendel JF. Epigenetic phenomena and the evolution of plant allopolyploids. Mol Phylogenet Evol. 2003; 29(3): 365–379. pmid:14615180
View Article
PubMed/NCBI
Google Scholar

[92] View Article

[93] PubMed/NCBI

[94] Google Scholar

[ref32] 32. Comai L. The advantages and disadvantages of being polyploid. Nat Rev Genet,2005; 6(11): 836–846. pmid:16304599
View Article
PubMed/NCBI
Google Scholar

[96] View Article

[97] PubMed/NCBI

[98] Google Scholar

[ref33] 33. Bueno ML, Pennington RT, Dexter KG, Yoshino Kamino LH, Pontara V, Mesquita Neves D, et al. Effects of Quaternary climatic fluctuations on the distribution of Neotropical savanna tree species. Ecography. 2017; vol. 40, no 3, p. 403–414.
View Article
Google Scholar

[100] View Article

[101] Google Scholar

[ref34] 34. Bosso L, Luchi N, Maresi G, Cristinzio G, Smeraldo S, Russo D. Predicting current and future disease outbreaks of Diplodia sapinea shoot blight in Italy: species distribution models as a tool for forest management planning. Forest Ecology and Management. 2017; vol. 400, p. 655–664.
View Article
Google Scholar

[103] View Article

[104] Google Scholar

[ref35] 35. Kaki E, Gilbert F. Using species distribution models to assess the importance of Egypt's protected areas for the conservation of medicinal plants. Journal of Arid Environments. 2016; vol. 135, p. 140–146.
View Article
Google Scholar

[106] View Article

[107] Google Scholar

[ref36] 36. Rovzar C, Gillespie TW, Kawelo K. Landscape to site variations in species distribution models for endangered plants. Forest Ecology and Management. 2016; vol. 369, p. 20–28.
View Article
Google Scholar

[109] View Article

[110] Google Scholar

[ref37] 37. G.tomentosa: GBIF.org (10th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.my22ws. G. struthium subs. struthium:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.dzjhbc. G. bermejoi:GBIF.org (11th November 2016) GBIF Occurrence Download http://doi.10.15468/dl.engt9m

[ref38] 38. Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. International journal of climatology. 2005; vol. 25, no 15, p. 1965–1978.
View Article
Google Scholar

[113] View Article

[114] Google Scholar

[ref39] 39. Gent PR. The community climate system model version 4. Journal of Climate. 2011; vol. 24, no 19, p. 4973–4991.
View Article
Google Scholar

[116] View Article

[117] Google Scholar

[ref40] 40. McCormack JE, Zellmer AJ, Knowles LL. Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation?: insights from tests with niche models. Evolution. 2010; vol. 64, no 5, p. 1231–1244. pmid:19922442
View Article
PubMed/NCBI
Google Scholar

[119] View Article

[120] PubMed/NCBI

[121] Google Scholar

[ref41] 41. R Core Team (2016). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/.

[ref42] 42. Broennimann O, Di Cola V, Guisan A. Ecospat: Spatial Ecology Miscellaneous Methods. R package version 2.1.1. 2016. https://CRAN.R-project.org/package=ecospat
View Article
Google Scholar

[124] View Article

[125] Google Scholar

[ref43] 43. Phillips SJ, Anderson RP, Schapire RE. Maximum entropy modeling of species geographic distributions. Ecological modelling. 2006; vol. 190, no 3, p. 231–259.
View Article
Google Scholar

[127] View Article

[128] Google Scholar

[ref44] 44. Phillips SJ, Dudík M. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography. 2008; vol. 31, no 2, p. 161–175.
View Article
Google Scholar

[130] View Article

[131] Google Scholar

[ref45] 45. Ferrandis P, Herranz J M, Copete MA. Caracterización florística y edáfica de las estepas yesosas de Castilla-La Mancha. Investigación Agraria: Sistemas y Recursos Forestales. 2005; vol. 14, p. 195–216.
View Article
Google Scholar

[133] View Article

[134] Google Scholar

[ref46] 46. Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ. A statistical explanation of MaxEnt for ecologists. Diversity and distributions. 2011; vol. 17, no 1, p. 43–57.
View Article
Google Scholar

[136] View Article

[137] Google Scholar

[ref47] 47. Merow C, Smith MJ, Silander JA. A practical guide to MaxEnt for modeling species’ distributions: what it does, and why inputs and settings matter. Ecography. 2013; vol. 36, no 10, p. 1058–1069.
View Article
Google Scholar

[139] View Article

[140] Google Scholar

[ref48] 48. Allouche O, Tsoar A, Kadmon R. (2006). Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). Journal of applied ecology, 43(6), 1223–1232.
View Article
Google Scholar

[142] View Article

[143] Google Scholar

[ref49] 49. Broennimann O, Fitzpatrick M C, Pearman P B, Petitpierre B. Pellissier L, Yoccoz NG et al. Measuring ecological niche overlap from occurrence and spatial environmental data. Global ecology and biogeography. 2012; vol. 21, no 4, p. 481–497.
View Article
Google Scholar

[145] View Article

[146] Google Scholar

[ref50] 50. Aguirre‐Gutiérrez J, Serna‐Chavez HM, Villalobos‐Arambula AR, Pérez de la Rosa JA, Raes N. Similar but not equivalent: ecological niche comparison across closely–related Mexican white pines. Diversity and distributions. 2015; vol. 21, no 3, p. 245–257.
View Article
Google Scholar

[148] View Article

[149] Google Scholar

[ref51] 51. Wiens JJ, Ackerly DD, Allen AP, Anacker BL. Niche conservatism as an emerging principle in ecology and conservation biology. Ecology letters. 2010; vol. 13, no 10, p. 1310–1324. pmid:20649638
View Article
PubMed/NCBI
Google Scholar

[151] View Article

[152] PubMed/NCBI

[153] Google Scholar

[ref52] 52. Thompson KA, Husband BC, Maherali H. Climatic niche differences between diploid and tetraploid cytotypes of Chamerion angustifolium (Onagraceae). American Journal of Botany. 2014; vol. 101, no 11, p. 1868–1875. pmid:25366852
View Article
PubMed/NCBI
Google Scholar

[155] View Article

[156] PubMed/NCBI

[157] Google Scholar

[ref53] 53. Glennon KL, Ritchie ME, Segraves KA. Evidence for shared broad‐scale climatic niches of diploid and polyploid plants. Ecology Letters. 2014; vol. 17, no 5, p. 574–582. pmid:24818236
View Article
PubMed/NCBI
Google Scholar

[159] View Article

[160] PubMed/NCBI

[161] Google Scholar

[ref54] 54. Hu J, Broennimann O, Guisan A, Wang B, Huang Y, Jiang J. Niche conservatism in Gynandropaa frogs on the southeastern Qinghai-Tibetan Plateau. Scientific reports. 2016; vol. 6, p. 32624. pmid:27601098
View Article
PubMed/NCBI
Google Scholar

[163] View Article

[164] PubMed/NCBI

[165] Google Scholar

[ref55] 55. Pearman PB, Guisan A, Broennimann O, Randin CF. Niche dynamics in space and time. Trends in Ecology & Evolution. 2008; vol. 23, no 3, p. 149–158.
View Article
Google Scholar

[167] View Article

[168] Google Scholar

[ref56] 56. Guisan A, Petitpierre B, Broennimann O, Daehler C, Kueffer C. Unifying niche shift studies: insights from biological invasions. Trends in ecology & evolution. 2014; vol. 29, no 5, p. 260–269.
View Article
Google Scholar

[170] View Article

[171] Google Scholar

[ref57] 57. Janžekovič F, Novak T. PCA–a powerful method for analyze ecological niches. En Principal component analysis-multidisciplinary applications. InTech. 2012.

[ref58] 58. Fernández-López J. 2017. NiceOverPlot, or when the number of dimensions does matter(R script).URL https://allthiswasfield.blogspot.com.es/2017/05/niceoverplot-or-when-number-of.html.

[ref59] 59. Schoener TW. Nonsynchronous spatial overlap of lizards in patchy habitats. Ecology. 1970; vol. 51, no 3, p. 408–418.
View Article
Google Scholar

[175] View Article

[176] Google Scholar

[ref60] 60. Warren DL, Glor RE, Turelli M. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution. 2008; vol. 62, no 11, p. 2868–2883. pmid:18752605
View Article
PubMed/NCBI
Google Scholar

[178] View Article

[179] PubMed/NCBI

[180] Google Scholar

[ref61] 61. García de Pedraza L. Fenómenos de estancamiento y Foehn. repositorio.aemet.es. 1972.
View Article
Google Scholar

[182] View Article

[183] Google Scholar

[ref62] 62. Capel Molina JJ. Factores del clima de la Península Ibérica. Paralelo 37.1978; no 2, p. 5–13.
View Article
Google Scholar

[185] View Article

[186] Google Scholar

[ref63] 63. Wiens JJ. Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution. 2004; vol. 58, no 1, p. 193–197. pmid:15058732
View Article
PubMed/NCBI
Google Scholar

[188] View Article

[189] PubMed/NCBI

[190] Google Scholar

[ref64] 64. Rieseberg LH, Willis JH. Plant speciation. Science. 2007; vol. 317, no 5840, p. 910–914. pmid:17702935
View Article
PubMed/NCBI
Google Scholar

[192] View Article

[193] PubMed/NCBI

[194] Google Scholar

[ref65] 65. Ehrlich PR, Raven PH. Differentiation of populations. Science. 1969; p. 1228–1232.
View Article
Google Scholar

[196] View Article

[197] Google Scholar

[ref66] 66. Rundle HD, Nosil P. Ecological speciation. Ecology letters. 2005; vol. 8, no 3, p. 336–352.
View Article
Google Scholar

[199] View Article

[200] Google Scholar

Figures

Abstract

1-Introduction

2-Materials and methods

2.1-Study area and species

2.2-Data sources

2.3-Maximum Entropy (MaxEnt) Model

2.4-Niche comparison

3-Results

3.1-Range changes in Gypsophila since Last Glacial Maximum (LGM)

3.2-Comparison of ecological niches

4-Discussion

5-Conclusions

Supporting information

S1 Table. Habitat suitability predicted by the MaxEnt models for G. struthium subsp. hispanica, during the Last Glacial Maximum, the Mid-Holocene and in the current climatic conditions measured at the points where the taxon is currently present.

S2 Table. As S1 but the values of suitability for G. struthium subsp. hispanica are taken at the current locations of its sister subspecies, G. struthium subsp. struthium.

S3 Table. Habitat suitability predicted by the MaxEnt models for G. struthium subsp. struthium, during the Last Glacial Maximum, the Mid-Holocene and in the current climatic conditions measured at the points where the taxon is currently present.

S4 Table. As S3 but the values of suitability for G. struthium subsp. struthium are taken at the current locations of its sister subspecies, G. struthium subsp. hispanica.

S1 Fig. Niche similarity test histograms.

S2 Fig. Niche equivalency test histograms.

Acknowledgments

References