Natural Poplar Hybrids I Continuous Variation of Foliar Characteristics
The importance of hybridization in the evolution of new species and introgression of genetic material from one taxon to another has long been recognized (Stebbins 1959). With the advent of sequencing and genomics technologies, hybridization and its impacts have become increasingly tractable for study and consequently, there is revived interest in the evolutionary and ecological significance of hybridization (Abbott et al. 2016). As hybrid species sit at the nexus of untangling the processes of evolution and ecological adaptation, their prominence in understanding biological diversity and species response to significant environmental change will continue to rise. In the current issue of Tree Physiology, Zanewich et al. (2018) report on the growth and physiology of natural hybrid poplars (Populus) raised under a range of temperatures to test their performance relative to the parent species.
For decades, studies have focused on the ability to produce phenotypic novelty in hybrid offspring (Yakimowski and Rieseberg 2014). Phenotypes of F 1 individuals are considered in the context of those observed in the parent species and are often assessed within an evolutionary or ecological framework (Stebbins 1959, Grant and Grant 1994). Frequently, the hybrid individual is found to possess an intermediate phenotype, falling between those of the parent species and implicating an additive genetic inheritance from both parents. Alternatively, the hybrid might exhibit a phenotype similar to that of one parent, suggesting genetic dominance. Hybrids may also show transgressive phenotypes where the hybrid phenotype falls beyond the normal range for either parent species. This is more often referred to in the literature as heterosis, and may be either positive or negative relative to both parent species (Stern 1948). Heterotic phenotypes, in either direction, primarily invoke a number of genetic mechanisms, such as overdominance, epistasis or 'complementary gene action' (Lippman and Zamir 2007, Birchler et al. 2010, Yakimowski and Rieseberg 2014). Collectively, these suggest that the hybrid individual has a combination of alleles that act to mask inferior or missing alleles and/or function in the same 'direction' to yield a superior (or inferior) performance. In some cases, a dosage effect may also be a component of heterosis, particularly in polyploid hybrids (Yao et al. 2013). Positive heterosis, more often referred to as hybrid vigour, remains the far more attractive field of study (at the time of writing 1.5 and 2.7× more articles can be found using 'positive heterosis' or 'hybrid vigour', respectively, compared with 'negative heterosis' on the Web of Science v.5.28 database) and arguments have been made for ignoring reduced or negative phenotypes (Birchler et al. 2010). Yet, understanding the full picture of positive and negative phenotypes in F 1 hybrids is necessary to inform the stability, adaptability and viability of hybrid-origin species. In addition, the question of plasticity in F 1 phenotypes under different environments is particularly relevant, especially for gaining insight into the persistence of natural hybrids, which is often associated with habitat modification and disturbance (Stebbins 1959, 1985).
Interspecific hybridization is more common in plants compared with animals, although the propensity to hybridize varies substantially by taxon (Stebbins 1959, 1985, Mallet 2005, Yakimowski and Rieseberg 2014). Willows and poplars (Salicaceae) have long been noted for their strong ability to hybridize. Natural interspecific hybridization within poplars is common and many hybrids are strongly persistent leading to taxonomically recognized hybrid species ( Eckenwalder 1984a , 1984b , 1996). In post-glacial North America, ranges of poplar species are often overlapping and hybridization within and between phylogenetic sections (a taxonomic rank between genus and species) is reasonably common in these areas. Many hybrid poplar species show a range of intermediate and heterotic phenotypes compared with the parent species (e.g., Gom and Rood, 1999). Notably, improved growth attributed to hybrid vigour (positive heterosis) has been observed in poplars originating from intersectional hybridization but not necessarily intrasectional hybridization (Rood et al. 2017). This may reflect the increasing evolutionary distance between taxonomic sections, which implies greater numbers of fixed differences between these lineages (Yakimowski and Rieseberg 2014).
The concepts of plasticity, stability and performance of hybrid phenotypes in taxa originating from an intersectional hybridization are brought together with new experimental evidence from Zanewich et al. (2018). In this study, cuttings from two riparian poplar species native to southern Alberta, Canada (Figure 1), Populus angustifolia (sect. Tacamahaca) and P. deltoides (sect. Aigeiros), and their naturally occurring hybrid P. × acuminata, were tested for temperature effects on growth and physiology under controlled conditions. The traits studied generally contribute to, or reflect, local adaptation in numerous poplar species (e.g., Dunlap et al. 1993, Gornall and Guy 2007, Soolanayakanahally et al. 2009, McKown et al. 2014, Kaluthota et al. 2015). Sizeable efforts are required to quantify large numbers of traits in numerous genotypes replicated across different temperature treatments. In Zanewich et al. (2018), applying this approach yielded novel insights into the nature and variability of hybrid phenotypes in relation to the parent species under different temperatures.
Figure 1.
Distributions of Populus angustifolia (sect. Tacamahaca) and P. deltoides (sect. Aigeiros) are shown in yellow and blue, respectively. Range overlap for both species is indicated in green. Location of P. angustifolia, P. deltoides and P. × acuminata from the riparian system in southern Alberta, Canada tested in Zanewich et al. (2018) is circled in red. The distribution map was created using the 'maps' package in R and shapefile data obtained from USGS (https://esp.cr.usgs.gov/data/little/).
Zanewich et al. (2018) illustrated that P. × acuminata exhibited positive heterosis in height growth, canopy mass and root mass primarily under cooler or suboptimal temperature treatment (15 °C). Interestingly, positive heterosis in these traits was not consistently observed but shifted to being intermediate or comparable to one of the parent species under higher temperature treatments. Among the physiological traits measured in P. × acuminata, the chlorophyll content index (often an indicator of foliar nitrogen and potential for carbon gain) showed intermediacy at the coolest temperature and similarity to the parent species with lower chlorophyll values at the warmer temperatures. Other physiological traits, such as nitrogen content (Narea), photosynthesis (A sat) and intrinsic water-use efficiency (WUEi), followed no consistent patterns with increasing temperature, exhibiting positive or negative heterosis, intermediacy or similarity to one parent. While lacking clear, directional trends with temperature makes interpreting effects on hybrid physiology more difficult, it also highlights the complex nature of phenotypes that are responsive to variable environmental conditions. Negative heterosis was consistently observed in stomatal density, regardless of temperature treatment, while the stomatal ratio (comparing stomatal numbers on both leaf surfaces) was consistently intermediate in the hybrid. Notably, the effects on stomatal conductance (g s) in P. × acuminata did not follow one trend or the other across temperature treatments, although the generalized pattern of g s in the hybrid was intermediate between both parent species.
The best illustration of relative hybrid performance in Zanewich et al. (2018) was provided by quantifying the degree of dominance and indices of change from the parent species for growth and physiological traits in P. × acuminata. It is clear from these estimates that improved growth in the hybrids and dispersion from the trait values of the parent species were primarily observed at the coolest temperatures. Zanewich et al. (2018) also report a number of trait–trait correlations, but data from the four temperature treatments are merged for each species and not tested separately. Given the potential for temperature effects on phenotypic outcomes, separate correlation analyses for each temperature treatment would be necessary to uncover changes in the relative strength and/or direction of correlative relationships for the hybrid and the parent species. Notably, the overall pattern for hybrid vigour in growth (at any temperature) was not mirrored in the photosynthetic physiology of P. × acuminata. This raises some uncertainty in the ability to sustain superior hybrid growth without enhanced rates of assimilation per unit area, particularly over the lifespan of a perennial plant (e.g., Pärnik et al. 2014). Previous reviews of physiology in hybrid crop plants also highlighted this phenomenon and identified the co-ordination of metabolism with environmental conditions, photosynthetic homoeostasis and stability with respect to temperature, and alignment in source–sink signals as physiological factors that are likely central to maintaining improved growth and yields in hybrids (Stuber 1994, Blum 2013).
The observation that hybrid traits are transitory and depend on environmental conditions not only underscores the gene by environment (G × E) implications but also highlights the plasticity of hybrid phenotypes. Among the traits quantified by Zanewich et al. (2018), only the stomatal data showed consistent patterns across all temperature treatments, signifying this as the only (observed) fixed trait between the parent species leading to predictable intermediate and negative heterotic phenotypes in the hybrid. Patterns in growth and physiological trait stability are less obvious. Many of these traits in other poplar species show continuous variation within natural populations and are only slightly to moderately heritable (Chamaillard et al. 2011, Keller et al. 2011, McKown et al. 2014), emphasizing the influence of the environmental component. As highlighted by Zanewich et al. (2018), the determination of intermediacy vs positive or negative heterosis in hybrids is relative and should be qualified by the environmental conditions under which they occur. This can be ecologically meaningful in estimating the potential survivability and/or competitiveness of F 1 hybrids vs their parent species in natural environments. For instance, positive heterosis for water-use efficiency became apparent only with increasing drought stress in a comparison of intersectional F 1 individuals from P. deltoides (Aigeiros) and Populus trichocarpa (Tacamahaca) (Braatne et al. 1992). Furthermore, the occurrence of negative heterosis, as observed in Zanewich et al. (2018), identifies environmental conditions under which the hybrid may perform more poorly than the parent species.
One factor that must be emphasized is that intersectional poplar hybrids, including P. × acuminata, possess the same ploidy as their parent species (Crawford 1974, Eckenwalder 1984a , 1984b ), and thus are likely the result of homoploid hybridization (i.e., no increase in ploidy of the hybrid individual). Hybridization has long been hypothesized to play an ecological role in accessing novel habitat types (Stebbins 1959, 1985), and homoploid hybrid species often occur in habitats diverging from those of the parent species (Yakimowski and Rieseberg 2014). Natural hybrid poplar species are commonly reported in habitats that are not occupied by the parent taxa (Eckenwalder 1996), although this is not the case for some areas, including the riparian study system in Zanewich et al. (2018). In general, homoploid hybridization is less associated with speciation due to a lowered potential for reproductive isolation (Schumer et al. 2014). This limitation can be overcome when homoploid hybridization is combined with sufficient physiological compatibility to novel habitats to effectively isolate the hybrid individuals (McKown et al. 2016). In poplars, the inability to achieve reproductive, physiological and/or environmental isolation likely plays a role limiting speciation following hybridization. Although poplars are dioecious, species in closely related taxonomic sections have the same sex-linked markers (Geraldes et al. 2015), suggesting that the limitation is elsewhere. Intersectional poplar hybrids have shown evidence for unidirectional introgression and asymmetric parentage, which could limit viability in F 2 individuals (Keim et al. 1989, Floate 2004, Hamzeh et al. 2007). There is also some evidence of selection against the recombinant genotypes of F 1 individuals from intrasectional hybridization in poplars (Christe et al. 2016).
Where no ecological separation exists between poplar hybrids and their parent species, the question of relative performance of the hybrid depending on environmental conditions remains. Comparative data from Zanewich et al. (2018) suggest that P. × acuminata only outperforms its parent species in the cooler, suboptimal conditions for the parent species. This finding is intriguing as populations of P. angustifolia and P. deltoides in southern Alberta are located near the northernmost (and possibly coolest) extent of their respective ranges (Figure 1). It is certainly possible that limited genetic material from homoploid hybridization (compared with a polyploid hybrid) influences the success of poplar hybrids, as loci underlying physiological and growth outcomes may have stronger effects. This may also contribute to phenotypic plasticity within hybrids where environmental inputs invoke differing responses in the individual parent species. There is the additional issue of divergence in growth and the supporting physiology in poplar hybrids. Future work disentangling the genetic basis of hybrid traits and incorporating the issue of homoploid hybridization are steps that should yield further insights into the nature of hybridization in poplars.
Conflict of interest
None declared.
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Author notes
handling Editor Danielle Way
© The Author(s) 2018. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com
© The Author(s) 2018. Published by Oxford University Press. All rights reserved. For Permissions, please email: journals.permissions@oup.com
Source: https://academic.oup.com/treephys/article/38/6/785/4999702
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