Determining the when, where and how of conifer speciation: a challenge arising from the study ‘Evolutionary history of a relict conifer Pseudotaxus chienii’

It is increasingly evident that the process of speciation does not strictly adhere to a simple model of vicariance among geographically isolated populations. Divergence often proceeds with varying levels of gene flow, natural selection and geographic isolation. Over the last few decades, an array of tools have been developed allowing us to more thoroughly investigate the multitude of ways in which species arise and the varying ways in which reproductive isolation evolves. For many lineages, there is a strong role of ecologically driven adaptation contributing to the evolution of reproductive isolation and hence the origin of new species (Hendry et al., 2007). Yet for others, geographically and ecologically separated populations comprise single species taxonomically housed within monotypic genera. In many of these instances, fossil evidence establishes these monotypic lineages as being quite old. The question becomes, why are these genera monotypic? In this issue, Kou et al. (2019) examine a relictual, monotypic conifer species, Pseudotaxus chienii (W. C. Cheng) W. C. Cheng, to test hypotheses about the role of geography and environment in driving divergence among populations and how this affects the process of speciation. They conclude that there simply has not been enough time for new species to arise due to the recency of divergence events in this lineage, as well as to a complex demographic history of gene flow and population size changes coupled to the lack of ecological divergence among populations. Here, we extend this thinking to a consideration of general mechanisms of speciation for conifers, the timing of which we feel is particularly apt given the explosion of genomics data for these charismatic plants.

Mechanisms driving speciation for conifers are not as well characterized as in other groups of plants despite a long history of crossing and common garden experiments. This is likely driven by their long generation times, large genome sizes, historical lack of genomic resources, and propensities to hybridize (Petit and Hampe, 2006). In the few detailed examples available (e.g. Mao and Wang, 2011), it is clear that there is a complex interplay among gene flow across populations (including hybridization), demographic processes within populations, and local adaptation to the formation of new conifer species. For conifers, we think this complexity is best thought of within models of ecological speciation (e.g. Mao and Wang, 2011).

Ecological divergence plays a major role in the establishment and maintenance of reproductive isolation in plants (Hendry et al., 2007), which suggests ecological speciation as a major generator of plant biodiversity. This model of speciation requires the build-up of reproductive isolation through ecological divergence among populations driving the development of prezygotic and postzygotic isolating mechanisms (Harvey et al., 2019). For conifers, prezygotic isolating mechanisms are often related to differential timing of phenological events (e.g. Zobel, 1969), while postzygotic isolating mechanisms are centred on hybrid inferiority due to genomic conflict resulting from the mixing of genetic material from ecologically diverged lineages (e.g. Manley and Ledig, 1979). In all cases, ecological divergence can be thought of in the context of the relationship between the fundamental and realized niches and how these evolve across populations, species and lineages. We argue, as do Pearman et al. (2008), that the relative time scales required for evolutionary processes to occur may be better understood if we looked through the kaleidoscopic lens of niche dynamics within and across lineages, as well as current and historical landscapes (Fig. 1).

Fig. 1.

Conceptualizing factors involved in speciation. (A) Interconnectivity among factors often considered during investigations related to niche evolution, adaptation and speciation. (B) Simple 2-D schematic showing the relationship between the realized niche (i.e. where the species is known to occur), the fundamental niche (i.e. where the species has the capacity to occur) and the hypothesized importance of divergent selection in the time needed for reproductive isolation to develop when all other factors from panel (A) are held constant. For the top two diagrams (i.e. stabilizing selection versus directional selection), imagine the niche spaces for two species are stacked on top of each other after completion of reproductive isolation. (C) Hypothesized relationship between environmental complexity and speciation rate. Open circles meet expectations. Closed circles may have life history traits or genetic architectures that are a deviation from expectations. (D) Hypothesized relationship between combined factors of standing genetic variation and environmental complexity on the probability of niche divergence. In environments with low complexity, the probability of niche divergence is low regardless of standing genetic variation. In homogeneous environments, it is hypothesized that niche stasis or niche directional shifts are more likely to occur than niche divergence.

In the case of Pseudotaxus chienii, despite a complex demographic history coupled to recent divergence events, there appears to be little niche divergence among populations, as isolation-by-environment was largely uncorrelated to genetic structuring among populations. Only a single climate variable (BIO8; mean temperature of the wettest quarter) was associated with this structure, which at face value may not necessarily disrupt reproductive compatibility. As argued by Kou et al. (2019), allopatry alone is unlikely to fuel speciation when divergence events are recent in terms of coalescent time units (e.g. 3–4 Ma) This is not to say that conservation of either the fundamental or realized niche impedes speciation, but that it likely slows the pace of it (Hendry et al., 2007). Kou et al. (2019) build upon this thinking to propose a related and testable hypothesis that speciation should be faster as spatial heterogeneity increases (Fig. 1C).

Simulation-based studies have tested similar hypotheses based on environmental heterogeneity (e.g. Schiffers et al., 2014), but empirical validation for conifers is lacking to date. The rates of adaptation, niche evolution and speciation are often affected by the same suite of interconnected factors (Fig. 1A), but due to the scope of variation housed within each factor it is unlikely that generalized predictions towards the rate of speciation and the development of reproductive isolation will emerge without further empirical and theoretical work. We do anticipate though that with a focused comparison of taxa sharing similar demographic histories, life history traits and geographical distributions, trends will emerge. Kou et al. (2019) point out the surprisingly dynamic nature common to several monotypic gymnosperms found in south-eastern China, which may be a fruitful place to begin.

For example, it may be the case that P. chienii experienced a reduction in realized niche breadth during founder events (Pearman et al., 2008), has constraints on niche evolution due to limited genetic variation (Schiffers et al., 2014), or that niche evolution within a more homogeneous environment (e.g. low landscape complexity with gradual, unidirectional changes in climate) has resulted in directional rather than divergent shifts in niche space (Fig. 1C). Additional constraints could include the presence of biotic interactions (e.g. competition; Pearman et al., 2008) and the genetic architecture of traits under selection (Schiffers et al., 2014). While the work of Kou et al. (2019) does not differentiate among these explanations for P. chienii, it sets the stage to rigorously link concepts from niche evolution theory, ecological speciation and evolutionary genetics to further our understanding of macroevolutionary trends within clades of plants, like conifers, where this knowledge is limited.

As argued above, one of the major keys to understanding mechanisms of conifer speciation is to think about niche evolution and its multifarious influences within a model of ecological speciation (Fig. 1). This is not to say that all speciation within conifers requires adaptive evolution, but that a modelling framework explicitly acknowledging this often-noted attribute of conifer lineages may be more illuminating than one without it, especially if the goal is to estimate the relative importance of factors contributing to species formation. Specifically, we propose three general questions, all of which could be tackled from theoretical and empirical approaches. First, while much work for conifers has focused on the relationship between genotypes and phenotypes for single species, relatively little of it has done so in a comparative evolutionary framework using genomic data. This is especially true for traits linked to reproductive isolation. For example, what are the phenotypic traits most often linked to changes in niche space for conifers, what are their architectures, and how do these architectures evolve across phylogenetic timescales to result in patterns of reproductive isolation? Second, given the pervasiveness of hybridization across conifer species, are there links among levels of local adaptation, genome structure and size, and ability to hybridize, and how do these relate to the evolution of prezygotic versus postzygotic reproductive isolating mechanisms? Lastly, how does spatial and temporal heterogeneity of selection pressures affect rates of diversification when populations within conifer lineages are far from any form of demographic equilibrium? For example, it is possible that the relatively slow diversification rates for conifers are tied to a mismatch among the timescales at which environments change, the time it takes for populations of conifers to adapt to environmental optima, and the time needed for reproductive isolation to evolve. This remains to be tested. We thank Kou et al. (2019) for their thought-provoking study that prompted the challenge now laid before us as a research community – determining the when, where and how of conifer speciation.

Funding

A.J.E. was supported by the National Science Foundation (NSF-EF-1442486).