Selbyana 19(1): 8-14

EVOLUTIONARY POTENTIAL IN ORCHIDS: PATTERNS AND STRATEGIES FOR CONSERVATION

JAMES D. ACKERMAN Department of Biology, University of Puerto Rico, PO Box 23360, San Juan, PR 00931-3360, USA

ABSTRACT. Strategies for species conservation should be based on at least two perspectives. First, one should know the demographic health of component populations which includes their growth, decline and interdependence. The second perspective, which I address here, is the maintenance of evolutionary potential, i.e., the ability to respond to change. This potential depends not only on patterns of variation but also on how populations differentiate. One model of evolutionary potential and differentiation in orchids is based on small population dynamics and repeated founder events. Species that show high levels of genetic vari­ ation within populations but little among them represent the pool of possibilities for future founding events which generate small populations. When variation is highest among populations. the potential for speciation is very high because populations are already differentiated to some degree, gene flow is minimal, and episodes of genetic drift and natural selection may be common. Conservation strategies can be very different for the two extreme patterns. For high variation within populations and little among them, the focus should be on conserving many individuals and this could be accomplished at one or few populations without substantial loss of genetic resources. When variation is greatest among populations then one must conserve as many viable populations as possible. Patterns of genetic variation can be revealed by molecular methods as well as standard morphometric techniques. Thus, the tools for estimating genetic resources are available to all and interpretation of the results are possible within existing theoretical frameworks.

Fundamental issues of biological conservation directly harvested or grazed in the wild (timber, are what to conserve and how to do it. One con­ medicinal plants, spices, ornamentals, food or cept that has permeated throughout the diverse forage); (2) used as sources for propagating ma­ field and into the realm of ecopolitics is "the terial (forage plants, wild relatives of crops, or­ conservation of genetic resources." The idea is namentals); (3) crucial for the well being of an not new nor was it intended to be restrictive ecosystem (dominant or keystone species or oth­ (Frankel & Bennett 1970), but it has gradually erwise crucial for the survival of other species expanded from cultivated plants to forest re­ that are of major concern); or (4) when desig­ sources and now to all taxa and levels of orga­ nated as endangered. Orchids could fit into any nization (Frankel et al. 1995) largely due to the one of these categories (except perhaps under realization that all species, no matter how seem­ the dominant or keystone species criterion). ingly insignificant, may have a profitability po­ When I last addressed the subject of orchid tential (cure for cancer!). conservation more than ten years ago (Acker­ Genetic resources are anything that contains man 1987), I focused on the extrinsic and demo­ functioning RNA and DNA (thereby excluding graphic factors that should affect orchid conser­ shampoos and hair rinses). Genetic resources are vation strategies. If one did not conserve the genes, organisms, and groups of organisms such habitat and mutualists of an orchid population as populations, species, and higher taxa. They (e.g., mycorrhizal symbionts, pollinators), then can also be viewed as ecologically interacting one would be in danger of conserving the living groups of species such as guilds and communi­ dead (Janzen 1986). It is clearly insufficient to ties. Which of these resources should be targeted save a species without saving its biology (e.g., for conservation? Species are usually the focus Cropper & Calder 1990). A rough indicator of and I shall argue that for species-targeted efforts, the status of a species and its mutualists is the population characteristics will guide the choice demographic health of its component popula­ of management strategies. tions. Individuals are immaterial except how their survival and reproduction affect popula­ Criteria for Conservation of Species tion-level processes. Thus, populations are the basic unit of species conservation. How do we identify orchid species worthy of concerted conservation effort? Although endan­ Minimum Viable Population gered or threatened species are the most dra­ matic cases, they are not the only taxa that Species become candidates for conservation should be targeted for conservation. Frankel et under the endangered or threatened categories al. (1995) point out that species should be prom­ when we perceive that their populations are at inent in conservation planning when they are (1) or below some minimum size for long-term sur-

8 1998] ACKERMAN: PATTERNS OF ORCHID POPULATION VARIATION 9 vival-a minimum viable population (MVP) tential (and genetic resources) of the orchid fam­ size. MVP is crucial to conservation planning ily are quite high. and may be defined as the minimum conditions Species richness in the Orchidaceae is often for the long-term persistence and adaptation of attributed to the plethora of pollination mecha­ a species or population in a given place (Soule nisms that have evolved in response to selection 1987). There are other definitions of MVP for cross-pollination fueled by the disadvantages (Frankel 1975, Schaffer 1981, Nunney & Camp­ of inbreeding. Darwin's (1885) monograph on bell 1993), but all have several features in com­ orchid pollination demonstrated the prevalence mon. First, MVPs are ecological and apply to of adaptations to enhance cross-pollination. A particular habitats for a specific time period. tradition was established and since then most They also attempt to incorporate genetic varia­ studies have emphasized mechanisms and "fit" tion and microevolutionary processes such as of orchid flowers to their pollinators (van der genetic drift, mating system, gene flow and nat­ Pijl & Dodson 1966). The marvels of orchid pol­ ural selection, all of which may affect the prob­ lination continue to pour into scientific journals ability of extinction. These factors are further (e.g., Vogel 1978, Ackerman 1983, Stoutamire influenced by random events including natural 1983, Kjellsson et al. 1985, Atwood 1985, Dafni catastrophes, both biotic (e.g., disease out­ & Calder 1987, Peakall 1989, Steiner 1989, breaks) and abiotic (e.g., volcanic eruptions, Johnson 1995); however, such adaptations are hurricanes, and droughts). the consequences, not the causes of evolution. With a demographic as well as an evolution­ Because all families of flowering plants have ad­ ary component, MVP assessment is not a simple aptations associated with the enhancement of matter. Long-term persistence or survival of cross pollination, such adaptations cannot ex­ populations under natural or managed conditions plain why some families are more diverse than are detected through population censuses, pro­ others. We need other criteria to explain why jectories of population health, extinction and re­ families such as the Orchidaceae, are more spe­ placement. The problems and procedures to ob­ cies-rich than others. tain these data are relatively unambiguous, but I propose that we draw our attention to pop­ answers may take many years of work to reveal ulations because all changes in species and high­ (e.g., Menges 1990, Tamm 1991, Waite & er taxa are a consequence of accumulated Hutchings 1991, Gill 1996). changes within populations. Evolution can only While the demographic component of MVP is occur if there is variation, and in the case of straightforward though potentially complex, the orchids, it is usually assumed that diversity is a evolutionary end of MVp, adaptation to chang­ consequence of natural selection playing on this ing environments, is without a doubt a tricky variation. Variation, then, represents evolution­ proposition. How does one characterize evolu­ tionary potential and what does one do to con­ ary potential. We expect that selection for cross-pollination serve it? In the following sections I discuss the evolutionary potential of orchids and relate it to would result in populations with a great deal of a model of evolutionary diversification. I shall genetic diversity. Assessments of genetic diver­ comment on the relationship between this poten­ sity in orchid species are scarce (about 1 in tial and rates of evolutionary change under con­ 2,000 species), but we do know that in outbreed­ trasting conditions of large and small population ing orchids, the levels of variation based on the sizes. Finally, I propose strategies for conser­ number of alleles per locus and different mea­ vation of the evolutionary potential of orchids. sures of heterozygosity are usually high (TABLE 1) relative to the average for monocots, short­ lived herbaceous perennials, widespread species, Evolutionary Potential of Orchids tropical species, animal-pollinated outcrossing The Orchidaceae is one of the most species species, and wind-dispersed species (Hamrick & rich families of flowering plants, perhaps the Godt 1990). However, most of our data come largest family of them all. Although some have from temperate terrestrial species and these may estimated that there are 30,000 species (Garay not be representative of most orchids, tropical 1960, Madison 1977), most recent accounts and epiphytic. place the number closer to 20,000 (Atwood If we assume that the evolutionary potential 1986, IDCN/SSC Orchid Specialist Group of orchids is and has been high, then under what 1996). Regardless of exactly how many species conditions has this variation been enhanced and there are, the orchid family is a major compo­ manipulated, resulting in an extraordinary spe­ nent of the world's flowering plant diversity, at cies diversity with a remarkable array of vege­ least in terms of the number of species. By the tative and reproductive adaptations? In the fol­ species richness criterion, the evolutionary po- lowing section I outline a model of diversifica- 10 SELBYANA [Volume 19(1)

TABLE 1. Genetic structure of orchid populations. A = Average number of alleles per locus; He = expected mean heterozygosity; Ht = total gene diversity; Hs = average gene diversity within populations; Gst = coefficient of gene differentiation among populations; Nm(S) = gene flow estimates (number of migrants per generation) based on Slatkin's private allele model; Nm(W) = gene flow estimate based on Wright's statistics.

Species Reference A He Ht Hs Gst Nm(S) Nm(W) Orchis morio Rossi et al. 1992 1.7 0.12 0.13 0.12 0.05 Orchis longicornu Corrias et al. 1991 1.9 0.16 0.23 0.22 0.02 4.2 3.7 Caladenia tentactula Peakall & Beattie 1996 0.031 Caladenia gemmata Peakall 1988 0.03 Drakea glyptodon Peakall 1988 0.09 Lepanthes rubripetala Tremblay 1996 0.40 0.29 0.31 0.48 0.75 Lepanthes rupestris Tremblay & Ackerman unpubl. 0.17 1.15 1.84 Lepanthes eltoroensis Tremblay & Ackerman unpubl. 0.22 1.54 0.89 LeporeUa jimbriata Peakall and James 1989 0.47 0.45 0.04 Microtis parviflora Peakall and Beattie 1991 0.30 Tolumnia variegata Ackerman and Ward unpubl. 3.6 0.2 0.20 0.70 0.09 8.0 2.50

1 Peakall and Beattie used Weir and Cockerham's !1l rather than Gst, but the results are usually equivalent. tion that should apply in principle to orchids as that are very different from the mean phenotype well as other families of flowering plants. of the parental population simply by chance (founder effect). These colonization events may Model of Orchid Diversification be common because orchid habitats are usually ephemeral (e.g., Benzing 1979, Ackerman 1983, In principle, large populations of outbreeding Case 1987) and the dust-like seeds of orchids species often contain substantial genetic varia­ carry a tremendous dispersal potential. With re­ tion so that one population may represent a sub­ peated founder events and numerous small pop­ stantial pool of evolutionary potential for a giv­ ulations, the effects of subsequent genetic drift en species. Large populations, on the other hand, as well as natural selection can be dramatic and may not be where all that potential is realized. effect rapid change, perhaps playing a major role Evolutionary change is expected to be slow ex­ in population differentiation and speciation (e.g., cept under catastrophic selection. On the other Wright 1931, Mayr 1954, Carson & Templeton hand, most of the total variation of a species 1984). Thus, the common condition of small should occur among its constituent populations population size in the orchid family represents a when these are small. Such populations lack the natural laboratory for genetic re-engineering evolutionary inertia of large ones, and when where popUlations may be subjected to episodes gene flow is limited, change can occur rapidly of genetic drift punctuated with bouts of strong through either genetic drift or natural selection. selection. The flip side of this scenario is that Thus, variation may be substantial in large pop­ although small populations may be the labora­ ulations, but rapid evolutionary change occurs tory for change, that change can also lead to in small ones. rapid extinction as well as diversification. The only model of differentiation in the or­ With this model, evolutionary potential may chid family based on these principles was reside in either large or small populations. There sketched by Gentry (1982), Gentry and Dodson are two basic patterns of variation representing (1987), Zimmerman and Aide (1989) and further endpoints of a spectrum of possibilities. In one, elaborated by Ackerman and Zimmerman most of the variation occurs within populations. (1994). It requires that effective population sizes Gene flow between populations is expected to (roughly the number of successfully reproducing be high so differentiation has not occurred (or is individuals) are small. This size effect is exac­ progressing very slowly). The other pattern is erbated in orchids because (1) nearly all species when most of the variation is among populations are severely pollination limited (Ackerman suggesting that populations have differentiated 1986), (2) often only a fraction of adults in a to some degree and gene flow is minimal. What population successfully reproduce (Calvo 1990), patterns do we see in the Orchid family? and (3) seed crops in orchids are often biparental rather than multipaternal. Colonization ability is Genetic Structure of Orchid Populations good but interpopulation gene flow is low. Be­ cause of small effective population sizes, new High levels of phenotypic variation within populations may be established by colonizers populations should yield high levels of genetic 1998] ACKERMAN: PATTERNS OF ORCHID POPULATION VARIATION 11 vanatlOn unless intrapopulation environmental potential of such species as very good, but pop­ heterogeneity and phenotypic plasticity are high. ulation change is either very slow or stagnant The extraordinarily variable Tolumnia variegata because gene flow counteracts the effects of lo­ is a weedy, obligate out-crosser found in Cuba, cal changes through genetic drift or natural se­ Hispaniola, Puerto Rico and the Virgin Islands lection. (Ackerman 1995). Plants are twig epiphytes and Gene flow among populations potentially oc­ average adult life expectancy is only a few years curs through both seed and pollen dispersal. (Melendez & Ackerman 1993). Recruitment is Some orchid pollinators, such as euglossine good even though plants are severely pollination bees, fly long distances (Janzen 1971, Ackerman limited and the proportion of individuals suc­ & Montalvo 1985) but interpopulation gene flow cessfully reproducing in a population can be is most often attributed to dispersal of the dust­ very small (Calvo 1993). A multivariate analysis like seeds. If gene flow is prevalent among or­ of morphological variation (Ackerman & Gal­ chid populations, then one must conclude that arza-Perez 1991) demonstrated that Puerto Ri­ the evolutionary processes in the family proceed can populations, regardless of their phenology at very slow rates, perhaps even slower than (spring or fall flowering), are more similar to most other groups of flowering plants (Soto Are­ each other than to populations in the Dominican nas 1996). This, of course, contradicts an axiom Republic or Cuba. Despite unsubstantiated of orchidology: the family is actively evolving claims to the contrary (Sauleda & Ragan 1996), and doing so at a rapid rate (Dressler 1981, Gen­ no combination of characteristics can separate try & Dodson 1987). So, which evolutionary the island populations as distinct taxa. Using scenario is correct? electrophoretic techniques to ascertain isozyme The answer is that both are correct. With more variation and to estimate gene flow, we discov­ than 20,000 species in the Orchidaceae, I expect ered that most allelic variation in T. variegata that the family contains a complete spectrum of of Puerto Rico and the Dominican Republic oc­ evolutionary states, from the hyperactive to the curs within populations (Ackerman & Ward in stagnant. Where do we look for indications of prep.). Population differentiation was insignifi­ evolutionary flux? Interspecific hybridization is cant (Gst = 0.09; 1 = completely different, 0 = a means of generating substantial variation and no difference whatsoever), and estimates of gene has been identified as one of the most important flow were very high, enough to overwhelm the means of diversification in flowering plants (e.g., effects of selection or genetic drift (Nm(S) = 8; Stebbins 1959, Arnold 1997). Hybrid zones are Nm(W) = 2.5). Genetic variation as measured where we expect to detect evolutionary process­ by expected heterozygosity and the effective es that mayor may not lead to speciation (Hew­ number of alleles per locus (TABLE 1) was higher itt 1988, Rieseberg & Wendel 1993). Certain than average for monocots, short-lived herba­ groups of orchids, particularly in Europe (e.g., ceous perennials, widespread species, tropical Orchis, Dactylorhiza), are subjected to these species, animal-pollinated outcrossing species, processes (e.g., Scacchi et al. 1990), but else­ and wind dispersed species (Hamrick and Godt where purported hybrid populations of orchids 1990). From any point of view, T. variegata is are too often ill-documented. Alternatively, we a very healthy species. Populations are large, should look at patterns of genetic variation gene flow is good, and levels of genetic varia­ among populations of species complexes and tion are higher than average. There is consider­ species-rich genera much as Gentry and Dodson able evolutionary potential, but because of gene (1987) suggested that we look at Anthurium, flow, evolutionary change is not likely to occur Piper and Cavendishia for indications of rapid rapidly (Sabat & Ackerman 1996, Ackerman et diversification. In the Orchidaceae, good candi­ al. 1997). If for some reason T. variegata should dates for such studies might be Bulbophyllum, become a candidate for conservation action, Dendrobium, Encyclia, Lepanthes, Maxillaria then an appropriate strategy for maintaining the and Oncidium. evolutionary potential of this species (based In the first detailed study to examine whether solely on genetic data) would be to conserve as or not the conditions for rapid diversification via many individuals as possible. This could be ac­ founder effects, drift and selection exist, Trem­ complished with one or a few populations with­ blay (1996) employed dispersion, morphology, out substantial loss of genetic resources. demographic and genetic assessments of Lepan­ Is the pattern of population genetic structure thes populations in Puerto Rico and discovered found in T. variegata common in other orchids? that both morphological and genetic variation The available data show that genetic variation is among populations of L. rubripetala were quite high, population differentiation is low and in­ high. In three species of Lepanthes, most sub­ ferred gene flow is substantial (TABLE 1). As in populations (individuals on separate phorophytes) T. variegata, one may regard the evolutionary differed significantly for many of the character- 12 SELBYANA [Volwne 19(1)

istics measured, even when the subpopulations of morphological variation mirror patterns of ge­ were separated by only a few meters. Genetic netic variation (at least for isozymes). If this re­ differentiation in L. rubripetala (the only species lationship holds, then one need not have a so­ studied at the time) was substantially higher (Gst phisticated laboratory to make a quick and rea­ = 0.31) than studies of other orchids (TABLE 1). sonable assessment of genetic variation. As expected when populations are well-differ­ Clearly, patterns of genetic variation are not entiated, estimates of gene flow were low (less all that one needs to know. I have emphasized than one migrant per generation) using both the importance of genetic variation in the con­ Slatkin and Wright's estimates (Nm (S) = 0.48; text of maintaining evolutionary potential but Nm(W) = 0.75). Under these conditions, both conservation is an issue because of ecological drift and natural selection may quickly alter the and demographic urgency. Genetic variation genetic structure and composition of these pop­ guides our choices for action, but one needs to ulations. Tremblay's data suggest that in this consider more immediate factors such as the ef­ evolutionary plastic genus, a great deal of vari­ fective population size, trajectory of population ation occurs among populations; therefore, the growth or decline, and potential for population appropriate conservation strategy to preserve the recovery. evolutionary potential is to target as many pop­ ulations as possible. Evolutionary action is in these small subpopulations, rarely connected by ACKNOWLEDGMENTS gene flow and subjected to genetic drift and lo­ I wish to thank Raymond Tremblay for shar­ cal selection. This scenario is not only akin to ing his ideas; Elvia Melendez-Ackerman for re­ various models of speciation that employ small viewing the manuscript; Sheila Ward and Wil­ effective population sizes (Wright 1931, Mayr liam Carromero for their laboratory expertise; 1954, Carson & Templeton 1984) but also to and numerous undergraduates for their assis­ those that emphasize the importance of meta­ tance in the field and laboratory. This work has populations in preserving variation and maxi­ been supported by grants NSF-RII 8903827, mizing rates of evolution (reviewed in Simber­ NSF-HRD 9353549 and NSF-DEB 9505459. loff 1988).

CONCLUSIONS LITERATURE CITED

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