Molecular Ecology (2014) 23, 20–22
NEWS AND VIEWS
PERSPECTIVE
Pollen, wind and fire: how to investigate genetic effects of disturbance-induced change in forest trees CECILE F. E. BACLES 25 rue Charles Floquet, 64100 Bayonne, France
Understanding the consequences of habitat disturbance on mating patterns although pollen and seed dispersal in forest trees has been a long-standing theme of forest and conservation genetics. Forest ecosystems face global environmental pressures from timber exploitation to genetic pollution and climate change, and it is therefore essential to comprehend how disturbances may alter the dispersal of genes and their establishment in tree populations in order to formulate relevant recommendations for sustainable resource management practices and realistic predictions of potential adaptation to climate change by means of range shift or expansion (Kremer et al. 2012). However, obtaining reliable evidence of disturbance-induced effects on gene dispersal processes from empirical evaluation of forest tree populations is difficult. Indeed, tree species share characteristics such as high longevity, long generation time and large reproductive population size, which may impede the experimenter’s ability to assess parameters at the spatial and time scales at which any change may occur (Petit and Hampe 2006). It has been suggested that appropriate study designs should encompass comparison of populations before and after disturbance as well as account for demonstrated variation in conspecific density, that is, the spatial distribution of mates, and forest density, including all species and relating to alteration in landscape openness (Bacles & Jump 2011). However, more often than not, empirical studies aiming to assess the consequences of habitat disturbance on genetic processes in tree populations assume rather than quantify a change in tree densities in forests under disturbance and generally fail to account for population history, which may lead to inappropriate interpretation of a causal relationship between population genetic structure and habitat disturbance due to effects of unmonitored confounding variables (Gauzere et al. 2013). In this issue, Shohami and Nathan (2014) take advantage of the distinctive features of the fire-adapted wind-pollinated Aleppo pine Pinus halepensis (Fig. 1) to provide an elegant example of best practice. Thanks to long-term Correspondence: Cecile F. E. Bacles, Fax: (33) 558 893871; E-mail: [email protected]
monitoring of the study site, a natural stand in Israel, Shohami and Nathan witnessed the direct impact of habitat disturbance, here taking the shape of fire, on conspecific and forest densities and compared pre- and postdisturbance mating patterns estimated from cones of different ages sampled on the same surviving maternal individuals (Fig. 2). This excellent study design is all the more strong that Shohami and Nathan took further analytical steps to account for confounding variables, such as historical population genetic structure and possible interannual variation in wind conditions, thus giving high credibility to their findings of unequivocal fireinduced alteration of mating patterns in P. halepensis. Most notably, the authors found, at the pollen pool level, a disruption of local genetic structure which, furthermore, they were able to attribute explicitly to enhanced pollenmediated gene immigration into the low-density firedisturbed stand. This cleverly designed research provides a model approach to be followed if we are to advance our understanding of disturbance-induced dispersal and genetic change in forest trees. Keywords: conservation genetics, habitat degradation, plant mating systems, population genetics—empirical Received 30 September 2013; revised 14 October 2013; accepted 18 October 2013
Pinus halepensis is a wind-pollinated, wind-dispersed conifer tree native to Israel and adapted to fire. Seeds are stored in serotinous cones that stay closed until hot and dry weather conditions, or fire, induce seed release. Sometimes, however, serotinous cones do not open under those conditions (Fig. 1). Shohami and Nathan cunningly used this feature in a natural stand of P. halepensis that had been severely disrupted by fire as a means to look into past—predisturbance—mating patterns. Indeed, they were able to classify cones on seven fire-surviving mother trees into three cohorts: ‘prefire’ corresponding to pollination occurring between 2 and 8 years before the fire, ‘early postfire’ with pollination occurring between 1 and 3 years after the fire and ‘late postfire’ with pollination occurring 8–10 years after the fire, covering a population dynamics span of at least 15 years (Fig. 2). This definition of three cohorts is essential to unequivocally relate mating patterns assessment to known population and landscape disruption monitored over the same period, including a 96% population reduction by the fire leaving just 13 surviving potential local pollen donors for the early postfire cohort, with an additional 30 saplings that had potentially reached sexual maturity in the recovering forest vegetation for the late postfire cohort. For each mother tree, pollen pool genetic composition was estimated by genotyping seven nuclear and three paternally © 2013 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 21
Fig. 1 These old serotinous cones stayed closed during a fire in a natural population of Aleppo pine, Pinus halepensis in Israel, providing a window into the past to assess prefire mating patterns of surviving trees and effective pollen dispersal within and outside the stand before habitat disturbance occurred. Photograph credit: D. Shohami.
Fig. 2 Cones of different ages on the same branch of an Aleppo pine, Pinus halepensis, tree with the youngest cones shown at the top (brown colour, 3 years old) and further down the branch older cones (approximately 1 year older for each whorl of cones from top to bottom: Counting annual growth rings within the branch allows for accurate age determination). Photograph credit: D. Shohami.
inherited chloroplast microsatellite markers from seeds from each cohort thus allowing to compare genetic differentiation (FST) and within-family relatedness (FS), that is, pollen being drawn from a limited number of donors, among the three disturbance-defined pollen cohorts. But where Shohami and Nathan’s approach is most remarkable is in their choice of © 2013 John Wiley & Sons Ltd
assessing pollen pool genetic structure separately for local (including self) and immigrant pollen by performing a simple paternity exclusion analysis of the surviving trees beforehand. This prior distinction of pollen sources is paramount in allowing the authors to identify that an observed randomization of mating in the early postfire cohort is due to immigrant pollen originated from unrelated donors outside the stand whereas local mating remains structured, whilst a return to structured nonrandom mating in the late postfire cohort could be attributed to an increase in apparent selfing once surviving trees had sufficiently recovered from the fire. Indeed, without such a distinction of pollen sources, the change in pollen pool structure and its link to disturbanceinduced change in pollen-mediated gene dispersal would have gone undetected because of strong historical genetic structure within the stand. The results of this study corroborate previous empirical research suggesting that pollen, and seed, -mediated gene flow (e.g. Bacles & Ennos 2008) could be enhanced in wind-pollinated, wind-dispersed tree species following disturbance-induced opening of the landscape and its associated reduction in conspecific density, but Shohami and Nathan provide for the first time the missing direct link between habitat-level disturbance and population and individual-level genetic parameters allowing to take interpretations beyond mere speculation. Two mechanisms have been put forward to explain enhanced gene flow in disturbed populations: The possibility of stronger winds in more opened landscapes allowing for longer distance dispersal, and lower competition for immigrant pollen due to a reduction in the number of local pollen donors. Given the high correlation between landscape opening and reduction in conspecific density, the debate on which of the two mechanisms is most important remains open, although recent research on wind-pollinated Fagus sylvatica using state-of-the-art mating models suggest a significant effect of canopy structure on pollen dispersal parameters at a local scale (Milleron et al. 2012, Gauzere et al. 2013). With their carefully crafted research, Shohami and Nathan demonstrate the importance of accounting for confounding variables in interpretation of genetic effects of disturbance in forest trees and is a sharp reminder of appropriate methodology in empirical assessment of genetic structure in disturbed tree populations. The unwanted consequences of misinterpretation of genetic effects for recommendations in forest management practices are too great for Shohami and Nathan’s approach not to be taken as standard, thus calling for long-term forest monitoring and generalization of the use of state-of-the-art spatially explicit mating models (e.g. Gauzere et al. 2013) in order to estimate mating parameters in the light of the genetic, ecological and environmental variables that characterize individual trees and population connectivity in changing forest landscapes.
References Bacles CFE, Ennos RA (2008) Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Heredity, 101, 368–380.
22 N E W S A N D V I E W S : P E R S P E C T I V E Bacles CFE, Jump AS (2011) Taking a tree’s perspective on forest fragmentation genetics. Trends in Plant Science, 16, 13– 18. Gauzere J, Klein EK, Oddou-Muratorio S (2013) Ecological determinants of mating system within and between three Fagus sylvatica populations along an elevational gradient. Molecular Ecology, 22, 5001–5015. Kremer A, Ronce O, Robledo-Arnuncio JJ et al. (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters, 15, 378–392.
Milleron M, Lopez de Heredia U, Lorenzo Z et al. (2012) Effect of canopy closure on pollen dispersal in a wind-pollinated species (Fagus sylvatica L.). Plant Ecology, 213, 1715–1728. Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annual Review of Ecology Evolution and Systematics, 37, 187–214. Shohami D, Nathan R (2014) Fire-induced population reduction and landscape opening increases gene flow via pollen in Pinus halepensis. Molecular Ecology, 23, 70–81. doi: 10.1111/mec.12569
© 2013 John Wiley & Sons Ltd
NEWS AND VIEWS
PERSPECTIVE
Pollen, wind and fire: how to investigate genetic effects of disturbance-induced change in forest trees CECILE F. E. BACLES 25 rue Charles Floquet, 64100 Bayonne, France
Understanding the consequences of habitat disturbance on mating patterns although pollen and seed dispersal in forest trees has been a long-standing theme of forest and conservation genetics. Forest ecosystems face global environmental pressures from timber exploitation to genetic pollution and climate change, and it is therefore essential to comprehend how disturbances may alter the dispersal of genes and their establishment in tree populations in order to formulate relevant recommendations for sustainable resource management practices and realistic predictions of potential adaptation to climate change by means of range shift or expansion (Kremer et al. 2012). However, obtaining reliable evidence of disturbance-induced effects on gene dispersal processes from empirical evaluation of forest tree populations is difficult. Indeed, tree species share characteristics such as high longevity, long generation time and large reproductive population size, which may impede the experimenter’s ability to assess parameters at the spatial and time scales at which any change may occur (Petit and Hampe 2006). It has been suggested that appropriate study designs should encompass comparison of populations before and after disturbance as well as account for demonstrated variation in conspecific density, that is, the spatial distribution of mates, and forest density, including all species and relating to alteration in landscape openness (Bacles & Jump 2011). However, more often than not, empirical studies aiming to assess the consequences of habitat disturbance on genetic processes in tree populations assume rather than quantify a change in tree densities in forests under disturbance and generally fail to account for population history, which may lead to inappropriate interpretation of a causal relationship between population genetic structure and habitat disturbance due to effects of unmonitored confounding variables (Gauzere et al. 2013). In this issue, Shohami and Nathan (2014) take advantage of the distinctive features of the fire-adapted wind-pollinated Aleppo pine Pinus halepensis (Fig. 1) to provide an elegant example of best practice. Thanks to long-term Correspondence: Cecile F. E. Bacles, Fax: (33) 558 893871; E-mail: [email protected]
monitoring of the study site, a natural stand in Israel, Shohami and Nathan witnessed the direct impact of habitat disturbance, here taking the shape of fire, on conspecific and forest densities and compared pre- and postdisturbance mating patterns estimated from cones of different ages sampled on the same surviving maternal individuals (Fig. 2). This excellent study design is all the more strong that Shohami and Nathan took further analytical steps to account for confounding variables, such as historical population genetic structure and possible interannual variation in wind conditions, thus giving high credibility to their findings of unequivocal fireinduced alteration of mating patterns in P. halepensis. Most notably, the authors found, at the pollen pool level, a disruption of local genetic structure which, furthermore, they were able to attribute explicitly to enhanced pollenmediated gene immigration into the low-density firedisturbed stand. This cleverly designed research provides a model approach to be followed if we are to advance our understanding of disturbance-induced dispersal and genetic change in forest trees. Keywords: conservation genetics, habitat degradation, plant mating systems, population genetics—empirical Received 30 September 2013; revised 14 October 2013; accepted 18 October 2013
Pinus halepensis is a wind-pollinated, wind-dispersed conifer tree native to Israel and adapted to fire. Seeds are stored in serotinous cones that stay closed until hot and dry weather conditions, or fire, induce seed release. Sometimes, however, serotinous cones do not open under those conditions (Fig. 1). Shohami and Nathan cunningly used this feature in a natural stand of P. halepensis that had been severely disrupted by fire as a means to look into past—predisturbance—mating patterns. Indeed, they were able to classify cones on seven fire-surviving mother trees into three cohorts: ‘prefire’ corresponding to pollination occurring between 2 and 8 years before the fire, ‘early postfire’ with pollination occurring between 1 and 3 years after the fire and ‘late postfire’ with pollination occurring 8–10 years after the fire, covering a population dynamics span of at least 15 years (Fig. 2). This definition of three cohorts is essential to unequivocally relate mating patterns assessment to known population and landscape disruption monitored over the same period, including a 96% population reduction by the fire leaving just 13 surviving potential local pollen donors for the early postfire cohort, with an additional 30 saplings that had potentially reached sexual maturity in the recovering forest vegetation for the late postfire cohort. For each mother tree, pollen pool genetic composition was estimated by genotyping seven nuclear and three paternally © 2013 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 21
Fig. 1 These old serotinous cones stayed closed during a fire in a natural population of Aleppo pine, Pinus halepensis in Israel, providing a window into the past to assess prefire mating patterns of surviving trees and effective pollen dispersal within and outside the stand before habitat disturbance occurred. Photograph credit: D. Shohami.
Fig. 2 Cones of different ages on the same branch of an Aleppo pine, Pinus halepensis, tree with the youngest cones shown at the top (brown colour, 3 years old) and further down the branch older cones (approximately 1 year older for each whorl of cones from top to bottom: Counting annual growth rings within the branch allows for accurate age determination). Photograph credit: D. Shohami.
inherited chloroplast microsatellite markers from seeds from each cohort thus allowing to compare genetic differentiation (FST) and within-family relatedness (FS), that is, pollen being drawn from a limited number of donors, among the three disturbance-defined pollen cohorts. But where Shohami and Nathan’s approach is most remarkable is in their choice of © 2013 John Wiley & Sons Ltd
assessing pollen pool genetic structure separately for local (including self) and immigrant pollen by performing a simple paternity exclusion analysis of the surviving trees beforehand. This prior distinction of pollen sources is paramount in allowing the authors to identify that an observed randomization of mating in the early postfire cohort is due to immigrant pollen originated from unrelated donors outside the stand whereas local mating remains structured, whilst a return to structured nonrandom mating in the late postfire cohort could be attributed to an increase in apparent selfing once surviving trees had sufficiently recovered from the fire. Indeed, without such a distinction of pollen sources, the change in pollen pool structure and its link to disturbanceinduced change in pollen-mediated gene dispersal would have gone undetected because of strong historical genetic structure within the stand. The results of this study corroborate previous empirical research suggesting that pollen, and seed, -mediated gene flow (e.g. Bacles & Ennos 2008) could be enhanced in wind-pollinated, wind-dispersed tree species following disturbance-induced opening of the landscape and its associated reduction in conspecific density, but Shohami and Nathan provide for the first time the missing direct link between habitat-level disturbance and population and individual-level genetic parameters allowing to take interpretations beyond mere speculation. Two mechanisms have been put forward to explain enhanced gene flow in disturbed populations: The possibility of stronger winds in more opened landscapes allowing for longer distance dispersal, and lower competition for immigrant pollen due to a reduction in the number of local pollen donors. Given the high correlation between landscape opening and reduction in conspecific density, the debate on which of the two mechanisms is most important remains open, although recent research on wind-pollinated Fagus sylvatica using state-of-the-art mating models suggest a significant effect of canopy structure on pollen dispersal parameters at a local scale (Milleron et al. 2012, Gauzere et al. 2013). With their carefully crafted research, Shohami and Nathan demonstrate the importance of accounting for confounding variables in interpretation of genetic effects of disturbance in forest trees and is a sharp reminder of appropriate methodology in empirical assessment of genetic structure in disturbed tree populations. The unwanted consequences of misinterpretation of genetic effects for recommendations in forest management practices are too great for Shohami and Nathan’s approach not to be taken as standard, thus calling for long-term forest monitoring and generalization of the use of state-of-the-art spatially explicit mating models (e.g. Gauzere et al. 2013) in order to estimate mating parameters in the light of the genetic, ecological and environmental variables that characterize individual trees and population connectivity in changing forest landscapes.
References Bacles CFE, Ennos RA (2008) Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Heredity, 101, 368–380.
22 N E W S A N D V I E W S : P E R S P E C T I V E Bacles CFE, Jump AS (2011) Taking a tree’s perspective on forest fragmentation genetics. Trends in Plant Science, 16, 13– 18. Gauzere J, Klein EK, Oddou-Muratorio S (2013) Ecological determinants of mating system within and between three Fagus sylvatica populations along an elevational gradient. Molecular Ecology, 22, 5001–5015. Kremer A, Ronce O, Robledo-Arnuncio JJ et al. (2012) Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters, 15, 378–392.
Milleron M, Lopez de Heredia U, Lorenzo Z et al. (2012) Effect of canopy closure on pollen dispersal in a wind-pollinated species (Fagus sylvatica L.). Plant Ecology, 213, 1715–1728. Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annual Review of Ecology Evolution and Systematics, 37, 187–214. Shohami D, Nathan R (2014) Fire-induced population reduction and landscape opening increases gene flow via pollen in Pinus halepensis. Molecular Ecology, 23, 70–81. doi: 10.1111/mec.12569
© 2013 John Wiley & Sons Ltd
