Climatic niche comparison across a cryptic species complex

Introduction

Ecological factors play an important role in speciation events by providing sources of selection that drive micro-evolutionary change and by imposing constraints that limit organism performance (Barrett & Hoekstra, 2011; Pyron & Burbrink, 2009; Rissler & Apodaca, 2007). If evolutionary lineages become geographically isolated during periods of climatic change, ecological components can also directly drive speciation. Nevertheless, species can also maintain their ancestral niche, which is referred to as niche conservatism (Wiens, 2004; Peterson, Soberón & Sanchez-Cordero, 1999; Peterson, 2011). The study of how species fluctuate in their requirements for and tolerance of such factors has advanced, in part, due to the continued theoretical development and quantification of the ecological niche of species (Soberón, 2007). Many methods have been proposed to test niche conservatism (Wiens, 2004) and define the climatic variables that constrain the distribution of species. Ecological niche modeling (ENM) is a relatively new method that has been used as a powerful tool to examine niche divergence and conservatism (Culumber & Tobler, 2016; Scriven et al., 2016). Spatially unequivocal environmental data and models allow for extensive scale tests about whether speciation is associated with niche divergence or whether closely related species tend towards niche conservatism (McCormack, Zellmer & Knowles, 2010). The development of ENM has promoted the extraction of ecological niche characteristics, which can help identity the niche limits of cryptic species (Wellenreuther, Larson & Svensson, 2012). Niche features have been applied to improve inferences about species boundaries and speciation mechanisms. Recently, a principal component analysis (PCA) method was present by Broennimann et al. (2012) that transforms the investigated environmental variables into a two-dimensional space identited by the first and second principal components. The niche overlaps value was measured by this approach that provides a relatively reliable way to test the niche divergence and niche conservatism hypotheses (Ahmadzadeh et al., 2013).

Cryptic species are a distinct but morphologically similar species that were classified as being a single one (Pfenninger & Schwenk, 2007). These species are not only important for taxonomic reasons, but also hold significant meaning in terms of biogeography (Pfenninger & Schwenk, 2007) and biodiversity (Oliver et al., 2009). The armored scale insects (Hemiptera, Diaspididae) are a family of over 2,650 described species according to current records (García et al., 2016). The Chionaspis pinifoliae heterophyllae species complex has only included two species, which are C. heterophyllae Cooley and C. pinifoliae (Fitch), since 1921 (MacGillivray, 1921). However, current reanalysis of species diversity within this group by Gwiazdowski et al. (2011) that suggested the presence of at least 10 closely related species, which have been delimited as cryptic species. These species are origin to North America (Vea, Gwiazdowski & Normark, 2012) and are considered pests on Pinus in forests and ornamental settings (Miller & Davidson, 2005). The adaptive deme formation (ADF) hypothesis proposes that a population may adapt to an individual host resulting in “a series of semi-isolated subpopulations, or demes” (Edmunds & Alstad, 1978). Many studies support ADF leading to multiple closely related cryptic species, such as armored scales (Anderson et al., 2010; Cook & Rowell, 2007). The result of research of Gwiazdowski et al. (2011) also supports this hypothesis. However, this study did not consider the ecological or climatic requirements of the species. Identifying the ecological niches of cryptic species is important to understanding the creation and maintenance of biodiversity (Oliver et al., 2009).

In the current study, ENMs and ordination techniques were used to characterize the ecological niches of the members of the Chionaspis pinifoliae heterophyllae species complex and test similarities between them. The main questions addressed in this study were: (1) What are the main environmental variables that constrain the potential distributions of members of C. pinifoliae heterophyllae? (2) Do cryptic species share the same ecological conditions? (3) What is the potential mechanism of geographic speciation of the allopatric and sympatric populations? The closely related species will result in high levels of similarity, ecological niche and spatial overlap. In addition, with niche divergence as a speciation mechanism, we would expect the ecological niches of closely related species to differ significantly. Because the cryptic species have similar morphological and physiological features, their ecological niches would be similar. However, because of the different adaptations to different environmental conditions, the non-equivalence of their ecological niches would be expected in the current study.

Methods

Study area and species

The Chionaspis pinifoliae-Chionaspis heterophyllae (CPCH) species complex inhabits across the USA, Mexico, and parts of Canada. Distribution data for CPCH were taken from Gwiazdowski et al. (2011). S3, S4, and S9 could not be included because of the low number of available sample locations (<5). Duplicate occurrences with the same geographic coordinates were removed using ENMtools software (Warren, Glor & Turelli, 2010). Occurrence records are often biased towards areas that are easily accessible or are near cities or other areas of high population density, thus, to remove spatial autocorrelation and the sampling bias, a grid of 5 × 5 km cells was created. A single point from each cell containing one or more sampling points was randomly selected. After filtering, 201 localities were retained in the final analysis, including S1 (29 points), S2 (21 points), S5 (8 points), S6 (22 points), S7 (22 points), S8 (13 points) and S10 (160 points). The distribution of the localities used in the study is presented in Fig. 1.

Results

Niche modeling and responses to climate variables

The partial ROC tests indicated a significant predictive ability for the models for all species (P < 0.001) (Fig. S2). The percentages of the variable contribution by members of the Chionaspis pinifoliae-Chionaspis heterophyllae species complex to the model construction are shown in Table 1. To visualize the suitable habitat areas of the species complex, model predictions were imported into a geographic information system and the areas were reclassified into two arbitrary categories of habitat suitability: unsuitable habitat (<threshold) and habitat suitability areas (threshold-1). The threshold is shown in Table 1. The distribution of the cryptic species is determined by different responses to the environment (Figs. 2 and 3).

Table 1:

The LPT threshold value of each model from MaxEnt.

Species	S1	S2	S5	S6	S7	S8	S10
Value	0.1779	0.509	0.586	0.580	0.305	0.540	0.029

DOI: 10.7717/peerj.7042/table-1

Notes:

Average LPT (Lowest presence threshold)

minimum training presence threshold

Suitable habitat areas for S1 were found at the high mean temperature of the driest quarter (Bio9) (−1–21 °C) and precipitation of the coldest quarter (Bio19) (200–5,000 mm). Both climate variables are the most important predictors for their potential distribution (Fig. 2 and Table 2). The mean temperature of the driest quarter (Bio9) was also an important environmental factor constraining the distribution of S2, with the highest suitability at values between 14.5 °C and 21 °C. The distribution of S5 was mainly constrained by the mean diurnal range (Bio2) (14.5–20.5 °C). S6 showed optimum suitability at the mean temperature of the wettest quarter (Bio8) (−5–5 °C) and at the mean temperature of the driest quarter (Bio9) (−3–31 °C). S7 was mainly constrained by the precipitation of the coldest quarter (Bio19) (100–900 mm). The mean temperature of wettest quarter (Bio8) was an important climatic factor constraining the distribution of S8, with the highest suitability at values between −2 °C and 12 °C. Suitable habitat areas for S10 were found for the mean diurnal range (Bio2) of 2 °C–15 °C, and the mean temperature of the wettest quarter (Bio8) of −20 °C–30 °C.

Relative to other environmental variables, temperature factors including mean diurnal range (Bio2) and mean temperature of the wettest quarter (Bio8) were the main factors affecting the distribution of this species complex.

Discussion

In this study, the environmental constraints for the current distribution of the members of the CPCH species complex were identified by applying ecological niche modeling and ordination techniques. The distribution range of the CPCH species complex in the North American continent mirrors the various environmental conditions to which they are adapted to. Additionally, they may also reflect the physiological differences between them. Temperature factors were the most significant limiting factor in the distribution of all CPCH. Higher temperatures could increase the fitness and abundance of the scale insect (Dale & Frank, 2017), thereby possibly increasing their chances of survival in extreme conditions.

Our results have shown that the distribution of each member of the CPCH complex is constrained by a set of environmental conditions. Climate change will directly affect the potential distribution of species, the ranges of which are strongly constrained by temperature and precipitation (Chen et al., 2011). The potential distribution of the members of the CPCH complex under climate change is not only limited by climate variables but also affected by other factors, such as species dispersal mechanisms, host-plant availability and human-mediated transport. The results provide a distribution range to facilitate the further control of these insects and formulate quarantine measures when an invasion by a member of this complex occurs.

Given the wide variation in the environmental conditions at locations where the members of the CPCH complex can be found, a low niche overlap between some members of this complex was expected. The low values of niche overlap between S1 and S7, S1 and S6, S2 and S6, and between S2 and S8, were also reflected in their different climate variable constraints. The result of the niche equivalency test between all pairs suggested a lack of ecological exchangeability. This result is in agreement with a previous study (Scriven et al., 2016) that morphological similarity does not necessarily equate to ecological equivalence. The result of the niche similarity test shows that the CPCH complex shares more climate niche characteristics than would be expected from random occurrence. In summary, the results show that there is a close relationship between these species, and they are likely to share climatic niche spaces. It is further confirmed that the members of the CPCH complex are closely related but are of different taxa. The differences in the environmental constraints of the different CPCH complex are also reflected in the niche similarity, overlap and equivalency results. In our analysis, the significant differences in the niche spaces reflect the reported taxonomic divisions within the CPCH complex (Gwiazdowski et al., 2011). Previous research has used differences in niches to support species delimitation (Aguirre-Gutiérrez et al., 2013; Raxworthy et al., 2007). Our results support the current species delimitation of the CPCH complex by molecular methods (Gwiazdowski et al., 2011; Vea, Gwiazdowski & Normark, 2012). These cryptic species are morphologically similar, but the climatic ecological characteristics have caused differentiation. Our results are consistent with other research that niches are similar but not equivalent across closely related species (Aguirre-Gutiérrez et al., 2013).

There are three traditional geographic categories for the phenomenon of speciation, which are allopatric (non-overlapping), sympatric (overlapping) and parapatric (adjoining) speciation, which depend on the degree of range overlap between species pairs during the speciation process (Zheng et al., 2017; Bultin, Galindo & Grahame, 2008). The speciation of different geographic categories was identified by the potential distribution modelling in recent studies. Our study supports the hypothesis that the niche overlap in the sympatric population was greater than that of the allotropic population (Hochkirch & Gröning, 2012).

Considerable overlap was found in the climatic niches of the different members of the CPCH complex (Table 3), such as S6 vs S8, S1 vs S5 and so on. These findings suggest that the divergent natural selection along climatic axes of the niche had played a limited role in the development of some pairs of this species complex. Many studies on a wide variety of taxa have suggested that ecological divergence plays an important role in sympatric populations (Via, 2001; Schliewen et al., 2001). Our results in the current paper suggest the lack of a large proportion of niche divergence between species pairs. These results are in accordance with the expectation that, given the climatic conditions available to them, closely related pairs will not be equivalent in their climatic niches, but will typically be more similar than expected. Our results agree with previous studies on the niche conservatism of sister species or species complexes (Graham et al., 2004; Silva et al., 2014). In our study, sympatric species pairs had very similar environmental niches or relatively high niche overlap, e.g., S6 vs S8 (Table 3, Fig. 2). This result suggests that these cryptic species likely experienced similar environmental pressures throughout their evolutionary history. Furthermore, the climatic niches are less likely to be influenced by competition and may thus represent interspecific differences in the fundamental niche. However, the larger niche overlap must lead to competition in sympatric and parapatric species pairs. Direct competition between these cryptic species is unlikely to exist (e.g., feeding), but there is potential competition for resources (e.g., host plants). The differences found in their use of forage plants may possibly be driven by competition and could reflect differences in their realized niches, rather than their fundamental niches.

Allopatric speciation is essentially a spatial process where two populations become genetically isolated due to geography, and thus the species pairs would have a relatively small niche overlap. The results of the current study suggest that some allopatric species pairs had a relatively small niche overlap, such as: S1 vs S6 and S1 and S8 (Table 3, Fig. 2). These results indicate that their niches belong to different environmental conditions. A hypothesis has been proposed that allopatric species may originate when a geographic barrier (i.e., an area of unsuitable environmental conditions between two sets of populations) develops faster than adaptation to these new ecological conditions. S1 is mainly distributed in southeastern North America and S6 located in western North America. There is a relatively large distance between the two species, with significant geographical isolation. Similarly, there is a larger geographic barrier between S1 and S8. In addition, the host plants of S1 are Pinus sylvestris, P. nigra, P. palustris, P. echinata, P. pungens, P. taeda, P. virginana, P. elliottiii, and P. rigida, while the host plants of S6 are P. torreyana, P. strobiformis, P. lambertiana, P. ponderosa, P. contorta, P. quadrifolia, P. attenuate, P. halepensis, P. jeffreyi, P. sabineana, and P. torreyana var. insularis. The host plants of S8 are Pinus undet, P. radiate, P. lambertiana, P. attenuate, P. ponderosa, P. contorta and Pseudotsuga menziesii. The species pairs have completely different host plants. Therefore, there may be a strict dietary isolation between the two species pairs. The distribution of host plants might determine the distribution of insects in our studies (Provencher et al., 2005). However, since populations on each side of the barrier would still have the same niche in cryptic species, it would have been niche conservatism that maintained the allopatric distribution. In our study, a small but clear overlap between the suitable areas defined by the ENMs of the allopatric sister taxa (Kozak & Wiens, 2006) would have been found. Our study also supports the hypothesis that niche conservatism may be generally important in allopatric speciation because it will limit adaptation to ecological conditions at the geographic barrier (Warren, Glor & Turelli, 2008). Parapatric species pairs (e.g., S2 vs S8, S5 vs S6, S2 vs S6) also show a relatively low niche overlap value. The underlying mechanism is similar to that of allopatric species distribution.

Conclusion

In summary, our results suggest that niche conservatism is common in this cryptic species complex and that these species occupy different climatic niches. The results suggest that allopatric species pairs had a relatively small niche overlap, which indicates that their niches are adapted to different environmental conditions. In addition, the results in our current paper suggest that there is a lack of a large proportion of niche divergence between sympatric species pairs. The results suggest that these cryptic species had likely experienced similar environmental pressures throughout their evolutionary history. In current study, the niche comparisons were implemented only using the Broennimann et al. (2012) method. However, other approaches, such as ENMtools (Warren, Glor & Turelli, 2010) or using more sophisticated methods of multivariate analysis, such as measures of the multidimensional overlap in species’ niche positions and breadths (Blonder et al., 2014) might provide much clearer results. Additional, only climate condition was consider in current work, however, other niche factor such as dispersal ability (Guisan & Thuiller, 2005), Interspecific interactions (Gao & Reitz, 2017) and host-plant availability (Ning, Wei & Feng, 2017) also affected the precision of the model. Thus, these factors should be consideration in future research.

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