Using species distribution models to locate the potential cradles of the allopolyploid Gypsophila bermejoi G. López (Caryophyllaceae)

Abstract

Polyploidy has been an influential force in plant evolution, playing a crucial role in diversification. Differences in polyploid and diploid distributions have been long noted, with polyploid taxa especially abundant in harsh environments. These plants have higher photosynthetic rates and/or higher tolerance to water deficits. Moreover, there is data pointing to an increase in the rate of unreduced gamete formation by plants under conditions of stress. Accordingly, a higher frequency of polyploid individuals would be expected in populations living under extreme environments, a phenomenon that may be relevant when considering the origin of allopolyploid species. Hybridization between distinct autopolyploids is known to produce allopolyploids and hence, a high frequency of compatible autopolyploids in an area could enhance the formation of stable populations of the corresponding allopolyploid hybrid. Here we consider the allopolyploid species Gypsophila bermejoi G. López and its parental taxa G. struthium L. subsp. struthium and G. tomentosa L. We have used Species Distribution Models to locate areas with low bioclimatic suitability for both parental taxa during the Last Glacial Maximum (LGM), hypothesizing that the rate of tetraploid hybrid formation would be higher than expected where low suitability areas of both parental species overlap. We selected those areas taking into account the strict gypsophyllic nature of these taxa. There is data pointing to a post-glacial origin of the current G. bermejoi populations and according to our hypothesis, such locations could be centers for hybrid tetraploid formation or potential cradles of this species. Indeed, potential Mid-Holocene cradles were also identified in this manner. The evolution of bioclimatic suitability in both LGM and Mid-Holocene cradles was studied to assess the possible survival of the hybrids, and the current distribution of G. bermejoi proved to be consistent with our hypothesis.

Fig 1. A possible mechanism of cradle formation.

We show two closely related species with an allopatric distribution. Both of them have a high suitability area around the centroid of their ranges (regions A and B in 1) and a lower suitability area (LSA) around their ranges (areas a and b in 1). According to a number of observations (see text), a higher frequency of autopolyploids (solid squares and circles) could be expected in the peripheral regions of both ranges (the LSAs). The LSAs will overlap if both species have some degree of sympatry and hence, there would be regions with a stronger presence of autopolyploids emanating from both species. This circumstance would favor the formation of fertile tetraploid hybrids (red triangles, species C in 3). We considered such areas as potential cradles or potential formation centers for the hybrid species. Such hybrids could also arise at other locations where the parental taxa could interbreed, although a lower rate of hybrid formation would be expected. This is a possible scenario for the speciation of G. bermejoi, where the A and B species would be its parental G. struthium subsp. struthium and G. tomentosa.

Fig 2. Low Suitability Areas (LSA) for G. struthium subsp. struthium and G. tomentosa.

To establish the intervals of low suitability, we need to know the suitability values predicted by the models at the locations where these taxa are present under current climatic conditions. For each taxon, we considered low suitability values to be all those between the minimum and the first quartile. We tried to assess the suitability values in which a high frequency of autopolyploids is expected for both species. In Fig 2A, the suitability value histograms for both taxa are shown, with the minimum and first quartiles indicated by colored lines. In interval 1 (the minimum between G. tomentosa and G. struthium subsp. struthium), there is low suitability for G. tomentosa but no presence of G. struthium subsp. struthium (making interbreeding impossible). In interval 2 (between the minimum and the first quartile of G. struthium subsp. struthium) there is low suitability for both taxa and according to our hypothesis, a higher frequency of autoplyploids might be expected. Interval number 3 has low suitability for G. tomentosa but not for G. struthium subsp. struthium. If we accept the situations for low suitability, there could be a higher frequency of G. tomentosa autopolyploids in this interval but not of G. struthium subsp. struthium. In these conditions a higher frequency of triploid individuals would be expected, which could also enhance the formation of the G. bermejoi tetraploid hybrid. As a consequence, we considered the 2+3 interval to be favorable for the formation of G. bermejoi, between the higher minimum (that of G. struthium subsp. struthium) and the higher first quartile (that of G. tomentosa). Fig 2B and 2D show the MaxEnt models during the LGM for G. struthium subsp. struthium and G. tomentosa, respectively, whilst Fig 2C and 2E show the LSAs for both taxa (suitability values between 0.07603 and 0.52207).

Fig 3. A digital version of the gypsum soils maps published by Mota et al.

(2011) was used to plot the sites of gypsum soils on the map (3A). During the LGM, the LSAs of the G. bermejoi parental taxa overlapped at some locations due to the high degree of sympatry of both taxa (yellow colored areas in 3B and 3C). According to our hypothesis, higher frequencies of autopolyploids and non-reduced gametes would be expected in those areas. The three taxa studied are strict gypsophytes and hence, we filtered all the gypsum outcrops included in the areas where the LSAs for both parental taxa (G. struthium subsp. struthium and G. tomentosa) overlap (3C). At those sites, there would be a higher probability of establishing thriving populations of the fertile G. bermejoi hybrid and thus, we consider such places as potential cradles for this species. 3D shows The overlapping LSAs of the parental G. bermejoi taxa during the MH period and (3E) the potential cradles for the same climatic period.

Fig 4. The bioclimatic suitability of G. bermejoi cradle locations in the LGM and Mid-Holocene periods were evaluated in the Mid-Holocene and current climate conditions.

The resulting statistical distributions were plotted as the dark blue histograms, while the pale blue histogram corresponds to the suitability values of the model at the sites the plant occurs under current climate conditions. The minimum value of this distribution was used as a survival threshold for this species. Comparing both histograms, we can see how many potential cradles maintain a bioclimatic suitability below this minimum and thus, G. bermejoi could not endure the climatic conditions at these sites. (4A) shows the comparison between G. bermejoi suitability values and those of the LGM cradles under Mid-Holocene climatic conditions and (4B) those for the current climatic conditions. (4C) compares the G. bermejoi suitablity values with those of the Mid-Holocene cradles during the Mid-Holocene and (4D) under current climatic conditions. In LGM cases (4A and 4B), the vast majority of cradles produced very low suitability values for G. bermejoi and it is difficult to consider the survival of this species at such locations. In contrast, for Mid-Holecene cradles it seems to be a number of surviving populations during that period (4C) and some of them to the present (4D).

Fig 5. Fate of the potential G. bermejoi cradles and expected current distribution of this plant according to our hypothesis.

The quaternary climatic oscillations over the past 25,000 years have produced dramatic changes in bioclimatic suitability for this species. (5A) Shows the LGM cradles where G. bermejoi populations are expected to survive during the MH and current (5B) climatic conditions. We repeated this analysis for the potential cradles produced during the MH period and the results are shown in (5C) and (5D). This approach enabled us to produce a predicted current distribution for G. bermejoi, assuming no dispersal from the original cradles. This expected current distribution is shown in (5E), along with the actual presences of G. bermejoi (red triangles).