Journal of 2012, 100, 76–87 doi: 10.1111/j.1365-2745.2011.01919.x

CENTENARY SYMPOSIUM SPECIAL FEATURE Evolutionary changes in plant reproductive traits following fragmentation and their consequences for population fitness

Hans Jacquemyn1*, Luc De Meester2, Eelke Jongejans3 and Olivier Honnay1

1Laboratory of Plant Ecology, University of Leuven, Arenbergpark 31, B-3001 Heverlee, Belgium; 2Laboratory of Aquatic Ecology and , University of Leuven, Charles Deberiotstraat 32, B-3000 Leuven, Belgium; and 3Institute for Water and Wetland Research, Department of Experimental Plant Ecology, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ, Nijmegen, The Netherlands

Summary 1. The effects of on plant population genetic structure and diversity are rela- tively well studied. Yet, most of these studies used molecular tools focusing on neutral genetic mark- ers, and much less is known about the potential evolutionary consequences of habitat fragmentation on ecologically relevant plant traits. 2. It can be expected that the altered biotic and abiotic conditions and limited gene flow following habitat fragmentation may impose strong selection pressures on traits important for plant fitness. Responses to these selection pressures may, however, be hampered by reduced through . Conversely, evolutionary changes in flower or dispersal traits may itself impact the strength of inbreeding and genetic drift. 3. In this review, we highlight different reproductive plant traits that may be under selection follow- ing habitat fragmentation, and we examine studies that have shown indications for rapid - ary responses. 4. There are still relatively few studies that have convincingly shown that habitat fragmentation generates rapid evolutionary responses. Separating genetic from plastic trait responses and quanti- fying the long-term fitness consequences of evolutionary changes in plant traits also remain major challenges. 5. Synthesis. Many plant traits may be subject to selection following habitat fragmentation, but, until now, studies that quantified evolutionary responses to habitat fragmentation are limited. To study the consequences of changing plant traits for population fitness, we advocate applying popu- lation models that link demographic vital rates, the responding plant traits and their heritability. Key-words: dispersal, habitat fragmentation, mating system, nectar, phenotypic variation, , selection

genetics and long-term viability of the residing plant species Introduction (Honnay et al. 2005; Broadhurst & Young 2007). Habitat loss and fragmentation, together with climate The population biological consequences of habitat fragmen- change, environmental degradation through pollution, the tation are driven by both direct and indirect effects of changes invasion of exotic species and , are consid- in and isolation. In a direct way, decreased ered to be the most important threats to population size may lead to the loss of alleles through genetic world-wide (Diamond 1989; Pimm & Raven 2000). The drift, and to increased homozygosity through inbreeding disintegration of large tracts of natural habitat into many (Wright 1931, Young, Boyle & Brown 1996) (Fig. 1, arrow 1). small and spatially isolated fragments has major and well- The increased spatial isolation may hamper gene flow between documented consequences for the population biology, plant populations and may therefore prevent the replenish- ment of alleles lost through drift, thereby increasing genetic dif- ferentiation between populations (Wright 1931; Franklin *Correspondence author. E-mail: [email protected] 1980). The impact of habitat fragmentation on population

2012 The Authors. Journal of Ecology 2012 British Ecological Society Habitat fragmentation and plant trait evolution 77

Ecologically relevant traits

6 3

Habitat 2 Ecological interacƟons and fitness components fragmentaƟon 4

5 7 1

Population genetic diversity

Fig. 1. Conceptual overview on how habitat fragmentation may drive changes in ecologically relevant plant traits. Arrows represent influences which can be positive or negative. Habitat fragmentation decreases population genetic diversity through genetic stochasticities (1). Habitat frag- mentation also affects ecological interactions in plant populations (for example interactions with pollinators) and may negatively affect fitness components such as seed set (2). Persistently altered ecological interactions may result in observable phenotypic changes in plant traits that have a genetic basis (3). In turn, these phenotypic changes may feedback to the population on an ecological time-scale (eco-evolutionary feedbacks, 6). Lowered population genetic diversity may, however, impede or slow down evolutionary changes of plant traits (4), or it may affect the fitness components of the populations (e.g. through inbreeding depression), or the ecological interactions within the population (5). Decreasing fitness and changing ecological interactions may in turn feedback on the genetic diversity of the plant population through what has been coined the vortex (7). genetic diversity and structure has been relatively well studied Herrera & Garcı´a 2010), mycorrhizal fungi (Peay, Garbelotto across a wide range of species. Although neutral genetic diver- & Bruns 2010), insect (Cagnolo et al. 2009) and sity cannot be directly linked to phenotypic variation, the parasites (Valladares, Salvo & Cagnolo 2006), all of which implicit assumption of many of these studies is that there is a may affect the dynamics and long-term viability of plant concomitant loss of quantitative together populations. with neutral genetic variation (Hoffmann & Willi 2008). Habitat fragmentation has a direct impact on a population Recent meta-analyses of this population genetic work have and often alters ecological interactions. Therefore, it is reason- clearly shown that habitat fragmentation lowers within-popu- able to expect that fragmentation exerts strong selection pres- lation genetic diversity through genetic drift (Leimu et al. sures that could potentially drive the evolution of ecologically 2006; Honnay & Jacquemyn 2007; Aguilar et al. 2008) and relevant plant traits in small and isolated populations (Fig. 1, inbreeding (Angeloni, Ouborg & Leimu 2011). However, not arrow 3). Moreover, the absence of gene flow between frag- all plant species are equally susceptible to loss of genetic diver- mented populations may facilitate such an evolutionary sity resulting from habitat fragmentation, and the extent of response (Merila¨ & Crnokrak 2001). The high genetic drift changes in local genetic variation is strongly mediated by plant typically observed in fragmented populations can facilitate a traits such as pollination mode and mating system (Aguilar two-phase process of in subdivided populations, as et al. 2008), or the presence of a persistent seed bank (Honnay proposed in the shifting balance theory of evolution (Wright et al. 2008). 1931). In the first phase, genetic drift causes each subpopula- Indirect effects of changes in population size and isolation tion to undergo a random walk in allele frequencies to explore are mediated by changes in interspecific interactions (Fig. 1, new combinations of alleles. In the second phase, a new arrow 2). Small and isolated plant populations have been favourable combination of alleles can become fixed by natural shown to experience problems with pollination and sexual selection and exported to other populations through migra- reproduction due to pollinator shortage, or to altered polli- tion. Evidence for the shifting balance theory of evolution nator behaviour and flight patterns (Aguilar et al. 2006). affecting mating system evolution was given by Barrett, Ness Especially in self-incompatible, dioecious or heterostylous & Vallejo-Marı´n (2009), who showed that the transition from species, the disruption of plant–pollinator mutualisms may outcrossing to selfing in the tristylous Eichhornia paniculata result in significantly lower reproductive success (Jacquemyn, was triggered by genetic drift and founder events, followed by Brys & Hermy 2002; Tewksbury et al. 2002; Kolb 2005; selective loss of outcrossing morphs and fixation of self-polli- Leimu et al. 2006). Similar effects can be expected for wind- nating variants. pollinated species as severe reductions in population density, On the other hand, evolutionary responses to habitat frag- which are likely to occur after have become frag- mentation may be hampered by a lack of sufficient genetic mented, have been shown to lead to substantial reductions diversity, resulting from drift and inbreeding (Fig. 1, arrow 4). in seed production (e.g. Jacquemyn & Brys, 2008; Hesse & If the genetic variation that is lost codes for phenotypic varia- Pannell 2011). Habitat fragmentation may also affect the tion, habitat fragmentation may impede adaptive responses interaction of plants with their animal seed dispersers (Levey (Stockwell, Hendry & Kinnison 2003; Leimu & Fischer 2008). et al. 2005; Gru¨ newald, Breitbach & Bo¨ hning-Gaese 2010; Moreover, decreases in population genetic diversity or changes

2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87 78 H. Jacquemyn et al. in genotype composition through drift may also have populations no longer find enough resources and ⁄ or nesting ecological effects, which may in turn affect the direction of the sites to complete their life cycle, leading to a gradual evolution of plant traits (Fig. 1, arrow 5). Ecological conse- decrease in the number of insect species in remnant patches quences of genetic diversity in plants have been demonstrated and in the population size of pollinators. Environmental at different levels of organization, from the population to the conditionsmayalsochangetosuchanextentthattheyare to the (Antonovics 1992; Hughes et al. no longer suitable to sustain populations of all insect species 2008; Bailey et al. 2009). For example, decreasing plant geno- that were present in intact patches, ultimately leading to typic diversity in fragmented plant populations may negatively strongly altered pollinator communities in fragmented habi- affect production or increase community invasibility tats. Given that insect populations are known to fluctuate (Booth & Grime 2003; Vellend, Drummond & Tomimatsu substantially from year to year, even under the best circum- 2010), directly affecting ecological interactions and possibly stances (e.g. Kalisz, Vogler & Hanley 2004), this may further evolutionary trajectories of plant traits. Finally, the suggestion increase the extent of pollen limitation in fragmented popula- that rapid evolutionary changes in phenotypic trait values, tions. With ongoing habitat alteration, climate change and occurring in the same time spectrum as ecological processes, agricultural chemical usage, changes in pollinator assem- may directly feedback to change the ecological interactions blagesareevenexpectedtoincreasefurtherinthenear and responses of the species (Schoener 2011) is represented by future (Ricketts et al. 2008; Winfree et al. 2009; Potts et al. arrow 6 on Fig. 1. These feedbacks between evolution and 2010). Ultimately, this can lead to losses of outcrossing plant ecology, both occurring at the same temporal scales, have been species that rely on pollinators for successful seed set (Bies- termed eco-evolutionary dynamics (Fussman, Loreau & meijer et al. 2006) unless species can adapt to the altered pol- Abrams 2007; Pelletier, Grant & Hendry 2009). linator environments. There is growing evidence that human activities can be asso- Whereas the ecological impact of habitat fragmentation on ciated with rapid evolutionary changes (Hendry & Kinnison plant reproduction has been well studied (e.g. Ashman et al. 1999; Palumbi 2001; Stockwell, Hendry & Kinnison 2003; 2004; Ghazoul 2005; Aguilar et al. 2006), relatively little Schoener 2011). But so far, potential effects of habitat frag- attention has been given to the potential evolutionary conse- mentation have not received the attention they deserve. In quences of anthropogenic disturbances on plant mating sys- plant species, high evolutionary rates (quantified by the units tems (Eckert et al. 2010; Harder & Aizen 2010). Theory Haldanes and Darwins) have been reported for plants adapt- suggests that of the pollination environment and ing to metal and herbicide tolerance, and to increased atmo- loss of specialist pollinators can generate diverse selective spheric ozone and CO2 concentrations (Bone & Farres 2001). forces on plant mating systems that are mainly driven by the Bone & Farres (2001) have provided considerable evidence extent and causes of pollen limitation (Lloyd 1992; Morgan that, for some plant traits, measurable evolutionary change & Wilson 2005; Eckert et al. 2010; Harder & Aizen 2010). may occur within 20 generations or less. They also found evi- However, it is difficult to predict which evolutionary trajec- dence for higher accumulation of evolutionary change in phys- tory a population or species will take when its pollination iological plant traits (such as heavy metal and herbicide environment becomes critically disturbed. In case of severe resistance) than in morphological traits (such as leaf length and chronic pollen limitation following habitat fragmenta- and biomass). tion, it is expected that floral traits are selected that either In this paper, we first review the available evidence on how promote outcrossing or provide autonomous self-fertilization habitat fragmentation may drive the evolution of ecologically and thus reproductive assurance. When pollinator relevant plant traits, focusing on reproductive traits and seed and pollinator limitation vary in space and time (Goodwillie, dispersal traits. Second, because the implications of altered Kalisz & Eckert 2005; Eckert et al. 2010), plants may evolve plant traits for population fitness are still poorly understood, to a mixed mating system. Under such a scenario, establish- we aim to clarify how demographic models can help to track ment of a delayed selfing mechanism will be most favourable, the long-term population-level consequences of micro-evolu- as it increases female fitness with little seed or pollen dis- tion. counting (Kalisz, Vogler & Hanley 2004). Additionally, floral that favour autonomous selfing are expected to act in the opposite direction of traits that are associated with Habitat fragmentation and plant mating the promotion of cross pollination, and therefore, changes in systems these two suits of traits may be closely linked. The abundance and diversity of pollinators in remnant frag- Although it is very likely that significant evolutionary shifts ments is likely to decrease as fragmentation increases (e.g. in plant breeding systems are currently happening in a large Sih & Baltus 1987; Aizen & Feinsinger 1994; Kearns, Inouye number of plant species inhabiting human disturbed habitats, & Waser 1998; Tewksbury et al. 2002; Krauss, Steffan-Dew- there are currently few reports on detectable responses of enter & Tscharntke 2003; Gonza´ lez-Varo, Arroyo & Apari- anthropogenic disturbances on plant trait evolution (Eckert cio 2009), which can lead to significant pollen limitation et al. 2010). A relatively long period of time may be required through reduced pollen deposition or lower pollen quality for significant floral adaptations to become detectable after (Ashman et al. 2004; Knight et al. 2005; Aguilar et al. 2006; populations have become fragmented, particularly in long- Yang, Ferrari & Shea 2011). In fragmented habitats, insect lived species. Evidence of human disturbances and habitat

2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87 Habitat fragmentation and plant trait evolution 79

inhabiting disturbed, pollinator-poor environments with 1.0 closely related congeners occurring in intact or optimal habi- tats. In response to anthropogenic disturbances, selfing and a concomitant reduction in flower size evolved three to four

) 0.8 m

t times more often than an increase in outcrossing. These results indicate that human-mediated disturbances can have profound 0.6 effects on mating patterns in plant species and most likely result in changes in plant traits that favour selfing. Increased levels of autonomous selfing may result from 0.4 reductions in the level of herkogamy or protogyny (Cruden &

Mean outcrossing ( Lyon 1989; Lloyd 1992; Morgan & Wilson 2005; Porcher & 0.2 Lande 2005). Eckert & Herlihy (2004) and Herlihy & Eckert (2007), for example, showed a significant increase of the autog- amous component of total selfing with decreasing herkogamy 0.0 in Aquilegia canadensis. Similarly, comparison of outcrossing Fragmented Undisturbed rates between populations occurring at the centre and the edge Type of their distribution range has shown that herkogamy was lower and selfing more prevalent in edge populations where Fig. 2. Mean outcrossing rates (tm) in seventeen plant species occur- ring both in fragmented and contiguous, undisturbed habitats (data natural pollinators were scarcer (Moeller 2006). In fragmented from Eckert et al. 2010). populations of the dune plant Centaurium erythraea,plants fragmentationonmatingstrategies in plant populations was growing in pollinator-rich environments had markedly higher reviewed recently by Eckert et al. (2010) and Harder & Aizen anther–stigma separation than plants growing in pollinator- (2010). Eckert et al. (2010) showed that in 17 species from poor environments (Fig. 3) (Brys & Jacquemyn 2011). At the same time, this reduction in the level of herkogamy was seven different families, the mean outcrossing rate (tm) was sig- nificantly (paired t-test, P = 0.004) lower in fragmented habi- associated with higher levels of autonomous selfing. Similar reductions in the level of herkogamy have been reported in tats than in undisturbed, contiguous habitats (tm = 0.753 and 0.820, respectively) (Fig. 2). Moreover, this study focused on fragmented populations of the Chiltern gentian (Gentianella trees and shrubs, with only one herb species included, suggest- germanica), in which the mean level of herkogamy was signifi- ing that this assessment may be more conservative in assessing cantly lower in small populations, probably associated with the effects of habitat fragmentation compared with studies that reductions in pollinator-mediated pollen deposition (Luijten focus on short-lived species. The effects are expected to be most et al. 1999). In heterostylous taxa, the transition from obligate pronounced in herbs, particularly monocarpic herbs, due to a outcrossing to selfing often involves the replacement of hetero- faster generation time and a more stringent need for reproduc- stylous variants, which are characterized by a heteromorphic tive assurance (Barrett, Harder & Worley 1996; Schoen et al. self-incompatibility system, with self-compatible homostyles 1997). Using a different approach, Harder & Aizen (2010) (e.g. Charlesworth & Charlesworth 1979; Barrett & Shore compared several pairs of related species in a number of genera 1987).

(a) (b)

Fig. 3. Flowers of Centaurium erythraea originating from populations occurring in two contrasting pollinator environments. (a) Plants from pollinator-rich environments have larger and more herkogamous flowers than plants from (b) pollinator-poor environments plants, which are characterized by smaller flowers that lack herkogamy (from Brys & Jacquemyn 2011).

2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87 80 H. Jacquemyn et al.

As autonomous selfing evolves, a concomitant selection fragmented habitats. Selection may therefore induce a shift for reduced investment in pollinator attraction (such as from iteroparity in undisturbed habitats to semelparity in dis- reductions in flower size, corolla diameter, number of flow- turbed habitats. The reverse may be true as well. Some species ers, floral longevity, etc.) and rewards (such as reduced nec- may benefit from the new environmental conditions in frag- tar and pollen production) is also likely to occur (Ornduff mented habitats and therefore increase the size of optimal 1969; Eckert et al. 2010). Plants of C. erythraea growing in flowering. pollinator-poor environments indeed had smaller flowers However, to our knowledge, there are no studies that have and fewer flowers per plant than plants growing in pollina- compared size-dependent flowering and evolutionary changes tor-rich environments (Fig. 3). Similarly, pollen-ovule ratios in optimal flowering size between fragmented and undisturbed, were significantly larger in plants occurring in pollinator-rich contiguous habitats. Wesselingh et al. (1997) showed that than in pollinator-poor populations (Brys & Jacquemyn threshold sizes for flowering were significantly different in the 2011). In this case, the lower pollen to ovule ratio in pollina- facultative biennial plant Cynoglossum officinale between pop- tor-poor environments was mainly caused by lower invest- ulations occurring in open dune habitats and in closed poplar ment in pollen production rather than by smaller ovule thickets. Similarly, Hesse, Rees & Mu¨ ller-Scha¨ rer (2008) numbers, confirming earlier findings that plants with a showed that threshold sizes for flowering in the clonal herb higher capacity of autonomous selfing allocate a smaller Veratrum album were significantly different between popula- amount of resources to traits that contribute to the male tions occurring in forests, hay meadows and pastures. These function relative to the female function (Lloyd 1987). results clearly indicate a pervasive influence of local habitat In the most extreme case, plants may loose their capacity to conditions on flowering behaviour and threshold sizes of flow- reproduce sexually and only regenerate by vegetative (clonal) ering and therefore suggest that habitat fragmentation can offspring. The balance between clonal reproduction and sexual affect the evolution of life histories of plant species. reproduction varies between different species, but also within In addition to effects on flowering, habitat fragmentation species, there can be extensive variation in clonal reproduction may also select for larger plant sizes, as larger plants are more (Honnay & Jacquemyn 2008; Vallejo-Marı´n, Dorken & Bar- attractive to pollinators than small plants. Using data from 16 rett 2010), which can often be related to deteriorating environ- populations, Weber & Kolb (2011) found that selection for mental conditions (e.g. Jacquemyn et al. 2005; Vandepitte increased inflorescence size decreased with increasing popula- et al. 2009). As habitat fragmentation may negatively affect tion size and density, suggesting that larger plants are particu- sexual function, this balance may shift in favour of clonal larly favoured in small plant populations, or in low-density reproduction (Rossetto et al. 2004), ultimately resulting in a populations. However, because the degree of pollen limitation degeneration of life-history traits associated with sexual repro- was independent of population size or density, the authors sug- duction (Eckert 2002). For example, in the aquatic herb gested that the observed selection gradients were mediated by Decodon verticillatus, Eckert & Barrett (1993) demonstrated local environmental conditions (light and base saturation). that populations had become infertile at the northern edge of Theoppositemayalsooccur,whenplantsaresusceptibleto the species’ range where populations only reproduce clonally. herbivores or pathogens. In this case, habitat fragmentation may select for smaller plant sizes if fragmentation is associated with increased abundances of herbivores or pathogens. For Size at flowering and plant size example, in the Mediterranean herb Erisymum mediohispani- Habitat fragmentation may also affect the optimal timing to cum, Go´ mez (2003) found significant selection on flower num- reproduce because local environmental conditions and pollina- ber, reproductive stalk height, basal stalk diameter, petal tor environments are likely to change within fragmented habi- length and inner diameter of the flowers when herbivores were tat patches. Decreased light availability due to shrub absent. When ungulates were present, selection on floral traits encroachment, for example, led to larger threshold sizes for completely disappeared and selection strength on flower flowering in fragmented populations of the perennial orchid number and vegetative traits decreased. Orchis purpurea (Jacquemyn, Brys & Jongejans 2010). More- over, costs of flowering were higher in shaded populations, Nectar production whichresultedinathreefoldincreaseinthethresholdsizethat was required to flower for two consecutive years. Several To increase their reproductive success, most animal-pollinated studies have documented heritable variation for the timing of plants produce rewards to entice insect pollinators to visit their flowering and the number of flowering events (Law, Bradshaw flowers (Mitchell 1993). Nectar is by far the most common flo- & Putwain 1977; Wesselingh et al. 1997; Johnson 2007), sug- ral reward and primarily consists of water, sugars and amino gesting that both of these life-history traits may be prone to acids, although there is high variability in nectar composition selection and evolve in different ways depending on the degree between species (Baker & Baker 1975; Baker 1977; Petanidou of fragmentation and associated changes in environmental 2005). Nectar plays a crucial role in the interactions between conditions and pollinator environments. For example, lower plants and their pollinators and hence in mating success and survival in fragmented habitats due to altered environmental mating patterns. Important insights into the functioning of conditions (such as conditions resulting from increased edge nectar come from experiments adding nectar-surrogates to effects) may lead to a decreased optimal size of flowers in nectarless orchid species. For example, adding sugars to

2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87 Habitat fragmentation and plant trait evolution 81

flowers of Disa pulchra increased the number of flowers probed pollinators and increase the degree of sexual reproduction. by insect pollinators, the time spent on a single flower and the Concomitantly, this may increase self-pollination, resulting number of pollinia removed (Jersa´ kova´ & Johnson 2006). In in a loss of fitness through inbreeding depression. Exploring similar experiments, artificial supplementation of nectar to which factors tip the balance in these alternative evolution- flowers resulted in significantly higher seed set in the rewardless ary outcomes may lead to important insights into how Dactylorhiza sambucina (Jersa´ kova´ et al. 2008). habitat fragmentation shapes populations. Experimental High variability in nectar volume and composition is also modification of nectar composition, for example through observed within species (Klinkhamer & van der Lugt 2004; adding fertilizer, is likely a very promising way to proceed. Herrera, Perez & Alonso 2006; Canto et al. 2011). This variability is partly inheritable and partly regulated by envi- Seed dispersal ronmental conditions (Leiss, Vrieling & Klinkhamer 2004; Leiss & Klinkhamer 2005). Due to this phenotypic variation The dispersal of propagules between fragmented habitats is in nectar production and composition, its inheritability and essential as it allows both the recolonization of empty habitat the direct link between nectar production and plant reproduc- fragments and the survival of small populations through a tive success, it can be expected that nectar characteristics are rescue effect. Parallel to the observed loss of dispersal capacity subject to strong selective forces. Given the reduced pollinator in insect and bird species on oceanic islands (Carlquist 1965; abundance in small and isolated plant populations, individu- Roff 1990), it can also be expected that selection for genotypes als with high nectar production (or a specific chemical nectar with decreased dispersal ability is likely in small and isolated composition) are expected to have a strong selective advan- plant populations. The idea is that high dispersal is associated tage because they are more attractive to the scarce insect with increased mortality in fragmented habitats because diasp- pollinators than plants with limited nectar production. In oresendupinahostilelandscapematrixanddie.Asthereisa large populations with high abundances of pollinators, this trade-off between dispersal capacity and other life-history selective advantage will be absent. Work on Echium vulgare traits (e.g. seed size and associated competitive power of has indeed shown that individuals with high nectar produc- emerging seedlings; Soons & Heil 2002; Jakobsson & Eriksson tion receive more pollinator visits, but only in sparse popula- 2003; but see Skarpaas et al. (2011) for confounding environ- tions (Klinkhamer & van der Lugt 2004; Leiss & Klinkhamer mental effects on this trade-off), individuals with low dispersal 2005). This suggests that selection is possible and may result capacity will be favoured in isolated plant populations as they in different nectar characteristics in small vs. large plant can invest more in other fitness-related traits. Common garden populations. It is unknown whether the specific nectar com- experiments have indeed demonstrated that seed dispersal position (including both sugar and amino acid components) traits such as the length of the pappus can have a genetic basis is also affecting the attractiveness of individual plants, and and may undergo rapid adaptations (Imbert 2001; Riba et al. therefore, whether there are different selective pressures to be 2005). Studies on oceanic islands confirm this result, where expected on nectar production and nectar composition. reduced seed dispersal capacity has been reported for Cirsium The production of additional, or more attractive, nectar is arvense, Lactuca (Mycelis) muralis and Hypochaeris radicata not cost free, however. In addition to its energetic cost (Pyke (Cody & Overton 1996; Fresnillo & Ehlers 2008). However, 1991), the increased production of nectar and the subsequent compared to reported rates of physiological adaptation increased attraction and changing behaviour of pollinators (for example to heavy metals), the rates of evolutionary may incur considerable fitness costs through more self-pollina- change in seed morphology leading to enhanced dispersal were tion and associated inbreeding depression. This may be partic- found to be very low for the two latter species (Bone & Farres ularly severe in small and isolated populations where the risk 2001). of inbreeding depression is already considerable (Keller & If the reduction of seed dispersal ability in plant populations Waller 2002). Jersa´ kova´ & Johnson (2006) noticed more on oceanic islands is paralleled in terrestrial habitat fragments, self-pollination when flowers of the nectarless orchid Disa pul- the detrimental consequences of habitat fragmentation for chra were artificially supplemented with a sucrose solution. population viability and recolonization rates can be expected Johnson, Peter & A˚gren (2004) predicted that a to increase with time. In this case, evolutionary changes of towardsnectarproductionin the non-rewarding orchid Ana- plant traits feedback on population fitness components, for camptis morio would result in an initial four-fold increase in example through increasing inbreeding, which may ultimately pollinarium removal, but at the same time, a 40% increase in result in population extinction (Gyllenberg, Parvinen & Dieck- geitonogamous self-pollination occurred. Leiss, Peet & mann 2002). However, it is important to note that the response Klinkhamer (2009), on the other hand, could not report signifi- of a population within a habitat fragment may differ from that cantly higher selfing rates in E. vulgare individuals with high of established populations on oceanic islands because plant nectar production. populations in terrestrial habitat fragments may be subject to To summarize, two opposing selective forces may be rapid turnover and meta-population dynamics. Spatially expli- active on the volume of nectar and on the nectar composi- cit models have shown that if local extinction is so high that tion of individuals occurring in small and isolated plant pop- empty patches remain uncolonized for a long time, migration ulations. The production of higher amounts of nectar, or between habitat fragments will be evolutionarily favoured more attractive nectar, may increase attractiveness to instead of hampered, resulting in evolutionary rescue (Heino

2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87 82 H. Jacquemyn et al.

& Hanski 2001). Second, the degree of isolation of terrestrial of these changes may incur severe fitness costs and therefore habitat fragments is not that extreme as that of oceanic islands. may be maladaptive in the long term. In general, changes in Therefore, evolution towards higher dispersal capacity is possi- plant traits may result (i) from evolutionary changes that ble because, mainly for well dispersing species, dispersal costs appear to be adaptive in the short term, but in the long term remain relatively low. may lead to evolutionary suicide; and (ii) from evolution of The scarce empirical evidence so far clearly suggests that plant traits that increase survival in a fragmented landscape. there is selection against seed dispersal capacity in fragmented One example of the latter is the increased investment in nec- terrestrial habitats. Cheptou et al. (2008) showed that Crepis tar production, which may result in a temporary increase in sancta, a species with heteromorphic seeds, produced more seed set, but in the long term may translate into higher mor- non-dispersing seeds in highly isolated urban populations than tality rates of established individuals due to inbreeding in well-connected rural populations. Applying a quantitative depression or costs of reproduction. In addition, the pressure genetic model, the authors suggest that, under strong selection of one selective agent may be influenced by that of another. against seed dispersal, evolutionary changes are possible For example, pollinator-mediated selection was found to be within 5–12 generations. Riba et al. (2009) found evidence that disrupted by conflicting effects of plant enemies acting dur- seeds of Mycelis muralis had lower wind dispersal capacity in ing or subsequent to pollination (Go´ mez 2003). low connectivity landscapes, both at a landscape scale and The next important step would be to find out how changes larger interregional scale. Interestingly, these authors found no in plant traits affect the long-term viability of plant species in such a relation for populations at the northern edge of their fragmented habitats. To do so, comparative analyses of long- range in Sweden, likely resulting from the high dispersal capac- term demographic data between populations in fragmented ity of the individuals that reached the range margin. This and continuous habitats are required. The most accurate pic- clearly shows the importance of population history for the ture of the role of habitat fragmentation as a selective pressure potential of seed dispersal capacity evolution. ideally requires the consideration of the entire life cycle of the plant, including survival and fertility, as well as the ecological scenario in which all possible interactions occur (Metcalf & Implications for population fitness Pavard 2007). Demographic components of fitness and all pos- From the previous sections, it is clear that habitat fragmenta- sible interactions that affect demography can then be linked to tion may alter life-history traits that are important in govern- specific aspects of habitat fragmentation, such as fragment ing the reproductive success of plant populations and dispersal size, isolation, connectivity or . of seeds. To what extent this is already happening at a large One approach for studying the population impact of plant scale is not clear, however, because empirical evidence for habi- responses to habitat fragmentation is to construct a popula- tat fragmentation-driven selection remains rather scarce. From tion model that explicitly includes links between demo- the previous examples, it is also not always clear whether the graphic vital rates, responding plant traits and habitat trait changes are genetically based or whether they are a result fragmentation. Such hierarchical population models (Jonge- of phenotypic plasticity. In many cases, measuring plant traits jans, Huber & de Kroon 2010) can also include correlations in common garden environments during several generations to between traits and can be used to analytically quantify how purge maternal effects is required to exclude the possibility of much plant responses to habitat fragmentation contribute – phenotypic plasticity and to quantify heritability of the trait both directly and indirectly through correlations with other changes. The available data suggest that for some traits, there traits – to population dynamical parameters such as the net is a heritable genetic component to the observed phenotypic reproductive rate or the per capita population growth rate variation. For example, estimates of broad-sense heritability of (van Tienderen 2000). These sensitivity analyses can also be herkogamy based on the regression between parents measured used to calculate selection gradients for traits of individuals inthefieldandprogenymeasuredinthegreenhousegavea (van Tienderen 2000; Coulson et al. 2003). Using this heritability index H2 = 0.62 in the dune plant C. erythraea approach, Ehrle´ n&Mu¨ nzbergova (2009) showed that direc- (determined on progeny derived from selfing, R. Brys and H. tional selection on the start of flowering in the perennial herb Jacquemyn, unpublished data; see Fig. 3). Similar levels of Lathyrus vernus occurred via both mutualistic and antagonis- heritable variation in the level of herkogamy have been docu- tic interactions. However, these interactions acted in opposed mented in Mimulus guttatus (mean H2 = 0.58; Carr & Fenster directions and affected different components of fitness. 1994), Gentianella campestris (mean H2 = 0.86; Lennartsson Moreover, the effects of first flowering date on population et al. 2000), Datura stramonium (mean H2 =0.30;Motten& growth rates varied between years, showing negative selec- Stone 2000) and Aquilegia canadensis (mean H2 =0.42; tion is some years and positive or no selection in others. Herlihy & Eckert 2007). Regarding seed dispersal traits, Whereas the previous models use stage-based matrix Imbert (2001) showed that the narrow sense heritability of the models, we believe that evolutionary demography will also percentage of dispersing central achenes vs. non-dispersing benefit from the development of integral projection models peripheral achenes in Crepis sancta was 0.25. (IPMs) (Easterling, Ellner & Dixon 2000; Ellner & Rees 2006) When genetically based changes in plant traits occur rap- that use continuous, rather than discrete state variables. This is idly after habitat fragmentation has taken place, it is often important because many demographic vital rates are continu- unclear whether they are beneficial to a population as some ous functions (e.g. plant size), and demographic consequences

2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87 Habitat fragmentation and plant trait evolution 83 of changes in plant traits can therefore be best described with or an invasion wave approach. The latter integro-difference continuous functions (Jacquemyn, Brys & Jongejans 2010). equations approach was developed by Neubert & Caswell Moreover, IPMs allow the evolution of important life-history (2000) and can be used to analyse differences in the spatial strategies, such as the evolution of flowering strategies, to be spread of different populations (Caswell, Lensink & Neubert studied as functions of size and age. Although the majority of 2003; Jacquemyn, Brys & Neubert 2005; Jongejans et al. studies have been applied to monocarpic plants (e.g. Rees & 2008). This invasion wave approach was recently combined Rose 2002; Childs et al. 2003; Ellner & Rees 2006; Hesse, Rees with IPMs into a spatial integral projection model (SIPM) that &Mu¨ ller-Scha¨ rer 2008; Kuss et al. 2008; Williams 2009), includes both demography and dispersal with continuous state recent studies have extended the IPM approach to polycarpic and trait variables (Jongejans et al. 2011). Stochastic versions plants (T.E.X. Miller, J.L. Williams, E. Jongejans, R. Brys and of all these models are becoming available as well as tools to H. Jacquemyn, unpublished data). Because vital rate functions analyse transient dynamics in addition to asymptotic dynamics may vary between years, extending the IPM framework to (Caswell, Neubert & Hunter 2011; Schreiber & Ryan 2011). stochastic environments allows stochastic variation to be Another promising approach that does not involve plant incorporated into the calculation of population parameters traits, but analyses various aspects of demographic vital rate (Childs et al. 2004; Rees et al. 2004, 2006; Ellner & Rees 2007; differences between populations involves a recent extension of Metcalf et al. 2008). Rees & Ellner (2009) recently provided a stochastic Life Table Response Experiment (SLTRE) analyses very thorough outline of how to apply IPMs to stochastic envi- (Davison et al. 2010). These analyses are based on simple ronments using a mixed models framework. matrix models and on Tuljapurkar’s (1990) small-noise A few animal studies provide an exciting evolutionary approximation of stochastic population growth (SNA-LTRE; demography outlook of these hierarchical population models Davison et al. unpublished data; Jacquemyn et al. 2011). This using IPMs as modelling framework (Coulson et al. 2010). approach allows the quantification of contributions from: (i) For instance, Ozgul et al. (2010) used a long-term data set to mean vital rates, (ii) differential variability of vital rates, (iii) show how changes in various life-history components contrib- correlations between vital rates and (iv) elasticities of vital uted to larger body masses and increased population size in rates. As such, these four components provide important infor- yellow-bellied marmots. They showed that earlier mation about (i) gross differences in performance between from hibernation and earlier weaning of young led to a longer populations, (ii) responses of vital rates to environmental fluc- growing season and larger body masses before hibernation. tuations, (iii) demographic trade-offs or synchrony of stage To assess the role of phenotypic and genotypic variances in transitions and (iv) differences in local selection pressures. driving population dynamics of species, Coulson et al. (2010) Using this approach, Davison et al. (unpublished data) used developed models that generated insights into the joint fragmented populations of the perennial herb Anthyllis dynamics of populations, quantitative characters and life his- vulneraria to show that scaled contributions of elasticity were tory. Using the IPM framework, they developed a theoretical significantly larger in shallow (<10 cm) soils than in deep model that linked IPMs, the Price equation, generation length (>10 cm) soils, suggesting stronger selection pressures in pop- and heritability estimates. The key finding of their approach ulations occurring in sites with shallow soils. Given that was that changing any of the character-demography functions increased periods of thermal stress and drought are expected generated a wide range of eco-evolutionary dynamics. To to produce directional selection, these results thus suggest that apply these new approaches to plants, the heritability of the local selection pressures may be more important in shallow involved traits in the field must be known. However, parent– soils, where the growing environment is the harshest. Scaled offspring relationships are rarely known in plant demography contributions of variability also tended to be larger in deeper studies, and, to our knowledge, there are no studies that have soils, whereas contributions of correlation were not related to used these models for plants. We therefore argue that future soil depth. This can be explained by the fact that deeper soils research should incorporate the ecological and evolutionary maintain moisture longer into the dry season, whereas factors that drive population dynamics of plant species to get shallower soils dry out quickly. Deeper soils also spend more better insights into the evolutionary aspects of fragmentation of the year in high-moisture states and vary more between for plant species. Ideas exist to bridge the gap between genetic years based on annual rainfall. In contrast, shallow soils spend and demographic studies (Metcalf & Mitchell-Olds 2009), more of the year in low-moisture states and therefore vary less and we expect important theoretical and empirical progress in between years. Finally, the finding that correlation contribu- this field in the coming years. tions were not related to soil depth suggests that extreme Spatial dynamics are inherent to the study of the evolution- weather conditions affected correlations in similar ways, inde- ary effects of habitat fragmentation. We have already pendent of soil moisture content. discussed the effects of fragmentation on seed dispersal and gene flow. Dispersal components can be added to hierarchical Conclusions population models in a very similar way as demographic components (Jongejans, Huber & de Kroon 2010). The result- In fragmented habitats, three types of evolutionary responses ing spatial population models can be spatially explicit using are possible. Habitat fragmentation may (i) reduce population simulations or spatially implicit using either a meta-matrix genetic diversity through genetic drift, (ii) drive adaptive approach (Hunter & Caswell 2005) to study changes in plant traits and increase individual plant fitness in a

2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87 84 H. Jacquemyn et al. fragmented landscape or (iii) incur changes that at first sight Biesmeijer, J.C., Roberts, P.M., Reemer, M., Ohlemu¨ ller, R., Edwards, M., appear to be adaptive in the short term, but turn out to be Peeters, T., Schafferrs, A.P., Potts, S.G., Kleukers, R., Thomas, C.D., Settele, J. & Kunin, W.E. (2006) Parallel declines in pollinators and maladaptive in the long term, resulting in decreasing fitness insect-pollinated plants in Britain and the Netherlands. Science, 313,351– and in evolutionary suicide of the fragmented population. The 354. results presented here highlighted several plant traits that may Bone, E. & Farres, A. (2001) Trends and rates of in plants. Genetica, 112–113, 165–182. be subject to micro-evolutionary changes due to habitat Booth, R.E. & Grime, J.P. (2003) Effects of genetic impoverishment on plant fragmentation. However, direct evidence is still limited, and community diversity. Journal of Ecology, 91, 721–730. more research is needed to conclude that the observed changes Broadhurst, L. & Young, A. (2007) Seeing the wood and the trees – predicting the future for fragmented plant populations in Australian landscapes. Aus- in a particular trait reflect adaptations to the altered environ- tralian Journal of Botany, 55, 250–260. mental conditions imposed by habitat fragmentation or envi- Brys, R. & Jacquemyn, H. (2011) Effects of human-mediated pollinator impov- ronmentally induced plastic responses. Moreover, since erishment on floral traits and mating patterns in a short-lived herb: an exper- imental approach. , doi: 10.1111/j.1365-2435.2011. demographic data of the entire life cycle of species are still lar- 01923.x. gely lacking, there is very little evidence that the observed Cagnolo, L., Valladares, G., Salvo, A., Cabido, M. & Zak, M. 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2012 The Authors. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100,76–87