Demographic Shifts Related to Mycoheterotrophy and Their Fitness Impacts in Two Cephalanthera Species
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Ecology, 97(6), 2016, pp. 1452–1462 © 2016 by the Ecological Society of America Demographic shifts related to mycoheterotrophy and their fitness impacts in two Cephalanthera species RICHARD P. SHEFFERSON,1,6 MÉLANIE ROY,2 ÜLLE PÜTTSEPP,3 AND MARC-ANDRÉ SELOSSE4,5 1Department of General Systems Sciences, University of Tokyo, 3-8-1 Komaba, Tokyo 153-8902, Japan 2Laboratoire Evolution et Diversité Biologique, Université Paul Sabatier – CNRS, UMR5174, 118 route de Narbonne, 31062, Toulouse Cedex, France 3Institute of Agricultural and Environmental Sciences, Estonian University of Life Sciences, Street Kreutzwaldi 5, 51014, Tartu, Estonia 4Institut de Systématique, Évolution, Biodiversité (ISYEB - UMR 7205 – CNRS, MNHN, UPMC, EPHE), Muséum national d’Histoire naturelle, Sorbonne Universités, 57 rue Cuvier, CP50, 75005, Paris, France 5Department of Plant Taxonomy and Nature Conservation, University of Gdansk, Wita Stwosza 59, 80-308, Gdansk, Poland Abstract. Evolutionary losses of photosynthesis in terrestrial plants all originate in photosynthetic ancestors. The adaptive context under which this transition happens has remained elusive because of the rarity of plants in which both photosynthetic and non- photosynthetic forms exist as a polymorphism. Here, we report on demographic patterns in photosynthetic (“green”) and nonphotosynthetic (“albino”) individuals within populations of two such species, Cephalanthera damasonium and C. longifolia, which also acquire nutrition from their mycorrhizal hosts (partial mycoheterotrophy). We hypothesized that demographic shifts in albinos relative to greens would include compensatory patterns with respect to fitness, such that maladaptive changes to survival or reproduction would be adaptively countered by changes to other parameters, such as growth probabilities. We tracked individuals in two populations of C. damasonium for 3 yr, and in one population of C. longifolia for 14 yr. We then analyzed vital rates for both phenotypes using general linear mixed models (GLMMs) and multi- state capture mark- recapture models (CMR), and used these models to develop size-classified, function- based population projection matrices. We estimated fitness as the deterministic population growth rate λ( ) for each phenotype, and explored the impact of shifts in demographic patterns to albinism via life table response experiments (LTREs). Mortality differed between greens and albinos, but not similarly across species. Albinos generally sprouted less than greens, and flowered more when small but less at other times. Albinos typically had a higher probability of fruiting, although their lower flower numbers yielded lower numbers of fruits overall. Fitness did not differ significantly among phenotypes. Thus, we did not find significant evidence that albinism is adaptive or maladaptive; however, if in fact it is the latter, then we did find evidence of incomplete compensation for declines in survival and reproduction from growth transitions, particularly to small flowering size classes inC. damasonium, and to large vegetative size classes in C. longifolia. These patterns indicate some support for the idea that albinism may lead to the speciation of mycoheterotrophic plants. Key words: Cephalanthera; loss of photosynthesis; mixotrophy; mycoheterotrophy; Orchidaceae. INTRODUCTION carbon from nearby photosynthetic plants (Smith and Read 2008), or more rarely from soil organic matter Plants are most well- known for their photosynthetic (Martos et al. 2009). In temperate forests, mycohetero- capability. However, many species have lost the ability trophic species are particularly numerous in the to photosynthesize, or have evolved a greatly weakened Orchidaceae and Ericaceae (Leake 1994, Bidartondo ability to do so (Krause 2008). Such species include >400 2005, Merckx 2013). species of terrestrial plants that have developed other The loss of photosynthesis presents an evolutionary means to procure the carbohydrates that they need, such puzzle to plant biologists. Photosynthesis makes energy as the mycoheterotrophic plants (Leake 1994, Merckx relatively cheap, and so at least in principle it may prevent 2013). The latter use carbon from their mycorrhizal carbon from becoming limiting under many circum- partners, the soil fungi establishing symbioses with their stances (Roy et al. 2013). Thus, although many muta- roots (Smith and Read 2008), which in turn obtain tions can abolish it because it requires many genes for complex protein machineries (Gao et al. 2010), its loss Manuscript received 18 July 2015; revised 18 January 2016; accepted 2 February 2016. Corresponding Editor: L. S. Adler. may generally be selected against. However, the many 6 E-mail: [email protected] evolutionary losses of the trait suggest that some adaptive 1452 June 2016 MYCOHETEROTROPHY AND FITNESS 1453 context(s) can favor this loss. Since nonphotosynthetic, nonphotosynthetic genotypes under at least some condi- mycoheterotrophic plants often live in shady forest floors tions. However, the extreme rarity of species in which (Gebauer and Meyer 2003, Bidartondo et al. 2004, both photosynthetic and nonphotosynthetic forms exist, Selosse et al. 2004), and typically acquire carbon from particularly as a polymorphism within the same popu- mycorrhizal fungi (Selosse et al. 2002), the adaptive lation (Tranchida- Lombardo et al. 2010), has generally context of the loss of photosynthesis in mycohetero- prevented the examination of demographic differences trophs, and the maintenance of this trait, may be tied to between these phenotypes. Such comparisons between difficulty in acquiring carbon by photosynthesis. Thus, photosynthetic (hereafter “green”) and nonphotosyn- forest herbs may be more likely to develop heterotrophic thetic phenotypes (hereafter “albino”) within the same lifestyles than plants inhabiting other ecosystems, both species are ultimately required to infer fitness differences. due to the ecological context of interspecific plant com- Among orchids, some species phylogenetically close to petition for light in forests, and to the availability of other mycoheterotrophic species exhibit such a polymorphism. energy sources via ectomycorrhizal fungi. Indeed, the Interestingly, these green photosynthetic species are par- latter are efficiently provided through surrounding trees, tially mycoheterotrophic (they are also called ‘mix- which provide up to 20% of their photosynthates to ecto- otrophic’; Julou et al. 2005, Selosse and Roy 2009, mycorrhizal fungi (Smith and Read 2008). Selosse et al. 2016), a condition that allows pure albinos The evolutionary shift from photosynthesis to pure to survive (e.g., Selosse et al. 2004, Julou et al. 2005, mycoheterotrophy may also make growth and repro- Abadie et al. 2006, Roy et al. 2013, Gonneau et al. 2014). duction costlier in mycoheterotrophs. Growth and repro- Further, reproduction by seed appears strongly limited duction are theoretically costly to survival, and to current by energy limitations which might have to do with the and future growth and reproduction. Such costs rarely loss of photosynthesis (Bellino et al. 2014), while vege- exhibit themselves in the short- term in long- lived plant tative survival, and potentially clonal growth, do not species (Primack and Stacy 1998, Shefferson et al. 2006), appear to be impaired due to carbon acquisition from although high- resolution matrix methods like integral mycorrhizal fungi (Roy et al. 2013, Gonneau et al. 2014). projection models combined with long- term monitoring Here, we use two populations of C. damasonium and and high sample sizes can identify them (Jacquemyn et al. one of C. longifolia to ask: Is the evolutionary loss of 2010, Miller et al. 2012, Sletvold and Ågren 2015a,b). photosynthesis evolutionarily adaptive in mixotrophic Generally, costs are only observed when populations are species? We report data on green and albino individuals experimentally stressed or resource variability is of Cephalanthera damasonium and of C. longifolia to accounted for (Reznick 1992, Primack and Stacy 1998), address this question, and we explore demographic sim- or when large sample sizes allow the demographic effects ilarities and differences of these two phenotypes, inte- of individual histories to be dissected (Shefferson et al. grating demographic differences across the life cycle into 2014). However, the few studies of demography in myco- a comparison of fitness based on the deterministic pop- heterotrophs suggest that growth and reproduction may ulation growth rate. We ask whether the albinos and more commonly be costly. For example, the loss of pho- greens co-occurring in the same population have equiv- tosynthesis may favor sprouting only for reproduction, alent fitness. We further ask whether any albino traits since leaves serve no more nutritional or reproductive exhibit trends suggesting adaptive compensation for any function (Shefferson et al. 2011). Furthermore, with seemingly maladaptive differences, and test the latter carbon supply obtained heterotrophically, carbon may with life table response analysis (LTRE). be limiting much more than would be possible under a photosynthetic lifestyle (Bruns et al. 2002, Roy et al. METHODS 2013), and this may even limit vegetative growth at least some of the time in such plants (Merckx 2013). If a purely Study species and field sites mycoheterotrophic lifestyle is costly, then demographic patterns should shift to deal with these trade- offs. For We studied the long- lived herbaceous perennial