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Review TRENDS in Ecology & Evolution Vol.16 No.11 November 2001 623 Evolutionary ecology of carnivorous

Aaron M. Ellison and Nicholas J. Gotelli

After more than a century of being regarded as botanical oddities, carnivorous populations, elucidating how changes in fitness affect plants have emerged as model systems that are appropriate for addressing a population dynamics. As with other groups of plants, wide array of ecological and evolutionary questions. Now that reliable such as mangroves7 and alpine plants8 that exhibit molecular phylogenies are available for many carnivorous plants, they can be broad evolutionary convergence because of strong used to study convergences and divergences in ecophysiology and life-history selection in stressful habitats, detailed investigations strategies. Cost–benefit models and demographic analysis can provide insight of carnivorous plants at multiple biological scales can into the selective forces promoting carnivory. Important areas for future illustrate clearly the importance of ecological research include the assessment of the interaction between processes in determining evolutionary patterns. availability and drought tolerance among carnivorous plants, as well as measurements of spatial and temporal variability in microhabitat Phylogenetic diversity among carnivorous plants characteristics that might constrain growth and fitness. In addition to Phylogenetic relationships among carnivorous plants addressing evolutionary convergence, such studies must take into account have been obscured by reliance on morphological the evolutionary diversity of carnivorous plants and their wide variety of life characters1 that show a high degree of similarity and forms and habitats. Finally, carnivorous plants have suffered from historical evolutionary convergence among carnivorous taxa9 overcollection, and their habitats are vanishing rapidly. A major focus of future (Fig. 1). For example, flypaper (sticky) traps have research on this exciting group of plants should be directed towards strategies evolved independently in five eudicot families for their conservation and management. (, Roridulaceae, Byblidaceae, and ), and pitfall traps Carnivorous plants have fascinated evolutionary have arisen in three eudicot families (, ecologists, botanists and horticulturists for centuries. Nepenthaceae and Cephalotaceae) and one monocot Early investigators were reluctant to accept that family (). Most researchers have plants could consume and other small followed Darwin’s lead in considering the flypaper invertebrates1; Darwin2 provided the first detailed traps of , and the Droseraceae (sensu experimental evidence for carnivory in several stricto) to be homologous2. As recently as the late genera. Since then, approximately 600 of 1980s, researchers thought that all extant carnivorous carnivorous plants have been identified in plants were derived from a common ancestor1. six angiosperm subclasses, including both However, modern molecular data support multiple, and eudicotyledons3,4. Twentieth- polyphyletic origins of the carnivorous plants, and century botanists focused on describing the even flypaper traps within the traditionally anatomical specializations and physiological recognized family Droseraceae (including the sundew mechanisms associated with botanical carnivory1,5 genera and ) appear to be and identifying commonalities among the homoplasic. Phylogenetic analysis based on sequences carnivorous plants. In the mid-1980s, Givnish6 of the chloroplast MatK gene suggest that Droseraceae proposed a general cost–benefit model to explain the is polyphyletic and that Drosophyllum should be restriction of most carnivorous plants to well-lit, moved into its own family10. nutrient-poor, waterlogged habitats. Although Current placements of carnivorous families common ecological factors have led to some within broader angiosperm phylogenies have been evolutionary convergence, focus on ecological determined using chloroplast rbcL (Refs 3,11,12), similarities has obscured important evolutionary MatK (Ref. 10) and ORF2280 (Ref. 13) sequences, differences. Recent research on carnivorous plants nuclear ribosomal 18S RNA (Ref. 14) and internal Aaron M. Ellison* has highlighted these differences, which illustrate transcribed spacer (ITS) sequences11. For Dept of Biological the richness of ecological and evolutionary questions carnivorous taxa in three families within the Sciences, Mount Holyoke College, South Hadley, that can be approached with these plants. New Caryophyllidae, phylogenetic analyses suggest a MA 01075-6418, USA. research on phylogeny informs monophyletic origin (Fig. 2)10. Molecular techniques *e-mail: aellison@ interpretations of cost–benefit analyses for the have also resolved relationships among the mtholyoke.edu evolution of carnivory in plants, use of captured prey, Sarraceniaceae, Roridulaceae and Byblidaceae, Nicholas J. Gotelli tradeoffs between attracting versus prey, which had been grouped on the basis of Dept of Biology, and overall ecological effects of the carnivorous morphological analyses as sister taxa within the University of Vermont, 1 14 Burlington, VT 05405, syndrome . Recent studies also have successfully Rosidae . The consensus tree based on rbcL, ITS and USA. modeled the demography of some carnivorous plant 18S RNA sequences places the Sarraceniaceae and

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(a) (c) structures, such as bladders and pitfalls, also evolved from ancestors possessing simpler, flypaper type traps [i.e. Roridula (flypaper) – Sarraceniaceae (pitfall; Fig. 1d); Drosera (flypaper) – (pitfall); Byblis (flypaper; Fig. 1c); and the butterworts (flypaper; Fig. 1e) – (bladder; Fig. 1f)]3.

The adaptive value of carnivory The multiple, independent evolution of carnivory in diverse plant families suggests that it is an (d) adaptation to the low nutrient, bright, waterlogged habitats in which carnivorous plants occur6. Thus, the nutritional benefits of carnivory have been a traditional focus of research16. Givnish6 proposed a cost–benefit model that predicts that carnivory is adaptive only in nutrient-poor environments that are well lit and moist (Box 1). This model requires (b) both high light and wet conditions, because the photosynthetic costs to carnivory are thought to exceed the benefits in either shady or dry habitats. Benzing17 recently extended this model by allowing (e) for explicit tradeoffs between light, moisture and nutrient availability through litter (Box 1). Benzing’s model can provide a synthetic framework for recent data showing that carnivorous taxa vary in the amount of obtained through carnivory and in the production of carnivorous structures. Testing these models requires detailed measurements of the contribution of carnivory to the nutrient budget of (f) the plant, photosynthetic rates of carnivorous and noncarnivorous organs, the relationship between nutrient uptake and photosynthesis, and production rates of carnivorous organs.

Nutritional benefits of carnivory Schulze et al.18 used δ15 nitrogen (N) (Ref. 19) of and insects to show that carnivorous species differ significantly in their reliance on -derived nutrients (Table 1). In general, reliance on insect- derived N increases as carnivorous structures become Fig. 1. Photographs of Roridula as sister taxa closely related to the more elaborate (from sticky of Drosera spp. to carnivorous plant taxa, Ericales3,11,14, but locates Byblis near the Solanaceae the >1 m tall pitchers of the cobra lily Darlingtonia illustrating evolution within the Asteridae14. This conclusion supports californica); the northern within and 20 convergent characters recent morphological analysis of the phylogenetic purpurea being a notable exception to this pattern . across clades. (a) Drosera position of Byblis based on its embryology15. The two Plants themselves vary through time in the relative binata; (b) Nepenthes remaining eudicot families of carnivorous plants, contribution of insect-derived N to total plant rafflesiana; (c) Byblis filifolia; (d) Sarracenia Lentibulariaceae and Cephalotaceae, have been N content. In the four genera of pitcher plants purpurea; (e) Pinguicula placed respectively in the Lamiidae and Geraniales, (, Darlingtonia, Nepenthes and vulgaris; (f) Utricularia based on rbcL sequences3. Sarracenia), juveniles have nonfunctional pitchers, radiata. All photographs Sequence data also provide insights into the origins and derive their N from the soil and from insects by Aaron M. Ellison. and evolution of carnivorous structures, with some captured by older pitchers18. By contrast, young surprises. Although carnivory has long been considered functional pitchers that capture insects retain to be a highly derived character9, within the virtually all the nutrients that they derive from prey carnivorous of the Caryophyllidae (Fig. 2) and do not shunt nutrients to nonfunctional carnivory is a basal trait within the Droseraceae pitchers18. Similarly, new bladders of the aquatic (flypaper traps; Fig. 1a) that is retained in the common bladderwort do not Nepenthaceae (as pitfall traps; Fig. 1b), but is lost in catch prey21, but once functional bladders are the derived Ancistrocladaceae and Dioncophyllaceae produced in mid-summer, this species obtains ~50% (except in peltatum)10. In other of its N from captured prey and the remainder from unrelated families, more elaborate carnivorous the surrounding water22.

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photosynthesize and capture prey. Model predictions, Plumbaginaceae Nepenthaceae therefore, are based on an evolutionary switch from noncarnivory to carnivory in habitats with few Polygonaceae Ancistrocladaceae nutrients and abundant light. However, many carnivorous plants, including pitcher plants and bladderworts, produce leaves that photosynthesize Tamaricaceae Dioncophyllaceae but do not capture prey, or produce traps that photosynthesize little or not at all. Plants with Frankeniaceae Drosophyllum nonphotosynthetic carnivorous structures should have different cost–benefit functions and be under Simmondsiaceae Droseraceae different selective pressures from those with photosynthetic carnivorous structures only27. For example, butterworts have leaves that both TRENDS in Ecology & Evolution photosynthesize and capture prey. Plants that are supplemented by hand-feeding produce more Fig. 2. Consensus tree from bootstrap analyses of MatK sequences for the Caryophyllidae, with and digestive glands, and consequently retain more emphasis on carnivorous taxa10. Families in which all members are carnivorous are shaded in dark grey. prey on their sticky leaves, than do unfed controls29. The Dioncophyllaceae (purple) has lost carnivory in all but one , the monospecific Triphyophyllum In line with predictions, this response is strongly peltatum. This phylogeny, which agrees substantially with those derived from rbcL data58, illustrates two 29 general principles of carnivorous plant evolution: (1) that carnivory can be ancestral within a clade; and correlated with irradiance , in spite of the greater (2) that within a clade, sticky (‘flypaper’) traps are normally ancestral to other trap types (here, pitcher abundance of prey in shaded habitats. However, the traps of the Nepenthaceae). Reproduced, with permission, from Ref. 10. response to prey does not diminish in either Pinguicula or Drosera spp. as soil nutrients increase25,30. A small increase in the availability of insect- Bladderworts (Polypompholyx and Utricularia derived N (e.g. through supplemental feeding) can spp.) are aquatic carnivorous plants, but unlike the lead to a disproportionately large increase in the related butterworts, they have bladder traps ability of carnivorous plants to harness soil N or interspersed among photosynthetic leaves. Bladders reproduce16. Many carnivorous plants produce contain some chlorophyll, but in U. macrorhiza, they and primordia for year y + 1 in year y, and photosynthesize at half the rate of the leaves31. such ‘preformation’23 could have significant Cost–benefit models predict an inverse correlation demographic consequences for carnivorous plants. between bladder production and leaf production, a Preformation also means that fertilization prediction that is supported by observations on experiments must span multiple years to give U. gibba32 and U. foliosa33 but not by observations on reliable results on the effects of nutrients on growth U. macrorhiza34. Overall, cost–benefit models for the and fitness of carnivorous plants24,25. evolution of carnivory have provided a firm foundation for guiding research and interpreting results until Photosynthetic benefits and costs of carnivory now, but these models need some expansion to account Although nutritional benefits of carnivory have for the diversity and plasticity of carnivorous organs. been documented, the general predictions of the cost–benefit models for the evolution of carnivory Ecological conflicts with prey capture have not been well tested because there are few There should be strong selection for carnivorous measurements of the photosynthetic rates of plants to evolve effective mechanisms of attracting carnivorous plants, and even fewer of the prey, given their dependence on animal-derived responsiveness of these rates to additional prey nutrients (Table 1). Many plants attract insects to (Table 2). Overall, carnivorous plants have very low to effect pollination, and early work on prey

maximal photosynthetic rates (Pmax), often 50% or attraction in carnivorous plants emphasized the more lower than co-occurring plant species26,27. In potential for carnivorous structures to mimic insect- 35 addition, Pmax of butterworts (Pinguicula spp.) and pollinated flowers . Flowers of all carnivorous plants sundews (Drosera spp.) do not respond to prey are pollinated by insects, resulting in possible additions, suggesting that the cost-benefit analysis of conflicts between pollination and prey capture. 6 carnivory based on carbon economy (i.e. Pmax) alone However, the majority of carnivorous plants are long- is insufficient to explain the evolution of carnivory in lived perennials that also reproduce vegetatively, plants27. The increased vigor and sexual and asexual so that contributes nutrients to future reproduction resulting from prey additions suggests growth might offset reductions in set caused by that carnivory supplies substantial nutritional prey– conflicts. For annuals (some Drosera benefits independent of photosynthetic rate27–29. and Utricularia spp. and all Byblis spp.), resolution of these conflicts is more crucial. Nutrients, light and plasticity in the production of In many carnivorous plants, spatial or temporal carnivorous organs separation between flowers and traps36 promotes Cost–benefit models (Box 1) assume that plants are segregation of prey and pollinators. A notable either carnivorous or not, and that the leaves both exception is Pinguicula vallisneriifolia, in which

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Box 1. Two models for the evolution of carnivory

There is a tradeoff between photosynthetic costs and variety of light regimes, because of tradeoffs benefits that could lead to the evolution of carnivory associated with two other niche axes. Carnivory is in nutrient-poor habitats (Fig. I; reproduced, with extremely rare among bromeliads (two out of permission, from Ref. a)a. Givnish et al. hypothesize approximately 3000 species), which were the

that enhancement of photosynthetic rates (P1 and P2) inspiration for Benzing’s model. There are many resulting from the addition of nutrients as a result of other mechanisms for nutrient acquisition among carnivory should be more rapid, and have less of a bromeliadsb, which might explain why pitfall traps tendency to plateau in high-light and moist and associated carnivory are rarely employed

environments (P1) than in dry or shady ones (P2). among this large family of monocots. Bromeliads Carnivory should evolve when the marginal benefits also are much more water-stressed than are of an investment in carnivory exceed its own cost (C) carnivorous plants, which might generally place – that is, when the net profit curve (Fig. I dotted lines) them on the lower curve of the cost-benefit curve slopes upward near C = 0. proposed by Givnish et al.a

Litter (scarce to C (Cost) abundant)

P1 (Sunny, moist)

P2 (Shady or dry)

Photosynthetic profit P1 – C

P2 – C Moisture Photosynthetic cost (inefficiency) (wet to dry) associated with carnivory

Fig. I TRENDS in Ecology & Evolution Light (high to low) In a subsequent model, Benzingb hypothesizes

that there should be a switch from carnivorous, to Fig. II TRENDS in Ecology & Evolution tubular litter-based, to -plant bromeliads along three niche axes: moisture, light and litter (from which bromeliads derive nutrients) (Fig. II; References reproduced, with permission, from Ref. b). The a Givnish, T.J. et al. (1984) Carnivory in the bromeliad surfaces in Fig. II represent the point at which the reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist nutrient-poor costs of specialized leaf construction exceed their habitats. Am. Nat. 124, 479–497 marginal benefits. In contrast to Givnish et al.’s b Benzing, D.H. (2000) Bromeliaceae: Profile of an Adaptive model, Benzing’s allows for carnivory to occur in a Radiation, Cambridge University Press

flowers and the first functionally carnivorous leaves effectively than do thrips, which primarily effect self of the season are produced close together in both pollination. In shady habitats, only the small space and time37. Thrips and beetles are both the pollinators visit flowers, and the prey–pollinator most common prey and the most abundant flower conflict is more intense. visitors to P. vallisneriifolia, and experiments Two studies of the details of ultraviolet (UV) demonstrate that seed set in P. vallisneriifolia is reflection patterns in pitcher plant traps38,39 have also pollinator limited. Among individuals of led to new conclusions about the relationship between P. vallisneriifolia, there are strong correlations trap and flower attractiveness. Gloßner38 illustrates between the abundance of thrips or beetles present in UV reflectance patterns of both traps and flowers of flowers and traps (r = 0.98 and 0.74, respectively)37. the winged pitcher-plant Nepenthes alata, the Thus, there is a clear conflict in this species between butterworts Pinguicula gypsicola and P. zecheri, and attracting pollinators and prey, which recent the bladderwort Utricularia sandersonii. She shows research has shown is partially alleviated by habitat that, within these phylogenetically disparate groups, heterogeneity37. In sunny habitats, larger pollinators flowers and traps differ in size, shape and contrast, (bees and butterflies) also visit flowers but do not get and concludes that these species have evolved to trapped. These visitors cross-pollinate plants more prevent pollinators from becoming prey.

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Table 1. Relative contribution of insect nitrogen to total nitrogen content for contrast, N. gracilis capture more beetles, carnivorous plants hemipteran bugs, and total flightless prey. Trap type Growth habit Species Mean % insect Refs Moran et al. further conclude that these two nitrogen sympatric species are partitioning prey, a phenomenon observed in other mixed assemblages Bladder Aquatic Utricularia vulgaris 51.8 22 of carnivorous plants41,42. Terrestrial Polypompholyx multifida 21.0 55 Sticky leaf Rosette 26.5 56 Demographic models of carnivorous plants Rosette 19.6 55 Following on from the extensive studies of the effects Vine 54.2 55 of carnivory on the survivorship, growth and Vine Drosera modesta 34.5 55 reproduction of carnivorous plants, formal Vine 87.1 55 demographic analyses of these plants have recently been developed4,43,44. Such analyses integrate growth, Vine Drosera subhirtella 35.6 55 survivorship and reproduction responses to estimate Erect, low growing Drosera huegelli 57.3 55 the finite rate of population increase (λ) and other Erect, low growing 36.7 55 measures of equilibrium population structure. λ can be Erect, low growing 51.4 55 used to forecast future population size45 and has been Erect, tall 49.1 55 interpreted as an important measure of individual Erect, tall 47.2 55 fitness that could be maximized by natural selection46. Erect, tall 64.7 55 Models for the evolution of carnivory require fitness Pitcher Rosette Cephalotus follicularis 26.1 18 estimates for carnivorous plants growing under a (pitfall) Vine Nepenthes mirabilis 61.5 18 range of environmental conditions. Such tests are Rosette 76.4 18 still a long way off, but the output from demographic models of population growth of carnivorous plants Rosette sp. 79.3 18 could be used as input for testing such models. Rosette 59.8 18 Long-term field studies of individual leaf (ramet) Rosette 10.0 20 and entire plant (genet) demography are possible because the persistent leaves and rosettes of many Moran et al.39 describe UV spectra and pitcher carnivorous plants are easy to mark permanently. morphology for six species of Nepenthes, a dioecious, Most carnivorous plants have poorly developed pitcher-forming genus, with approximately and predicting their population dynamics should not 80 palaeotropical species. In the lowlands of be complicated by temporal variation in :shoot northwest Borneo, N. rafflesiana and N. gracilis often ratios. They also rarely develop persistent seed grow together and potentially compete for the same banks47 so oscillations and time lags are not induced prey resources. Of the two, there is a significantly by delayed germination. Many carnivorous plant greater contrast in N. rafflesiana between the populations are endangered or threatened48,49, and peristome (the attractive lip of the pitcher that is well quantitative demographic analyses are needed to endowed with extra-floral nectaries) and the pitcher forecast their risk of extinction50. Because of their body in spectral reflectance wavelengths (UV, blue rapid responsiveness to variation in air-, water- and and green) that are most attractive to insects. soil-borne nutrient levels4,51, carnivorous plants Nepenthes rafflesiana also has larger pitchers than might be especially useful for understanding does N. gracilis, produces a sweet, attractive risks in the face of long-term fragrance40 and is more successful at catching flower- environmental change52, including chronic visiting insects: bees, moths, flies and thrips. By N deposition4 and global climate change. A recent study by Brewer44 demonstrates the power

Table 2.Average mass-based maximum photosynthetic rates (Pmax) and of a demographic analysis of population growth of photosynthetic nitrogen use efficiencies (PNUE) for carnivorous plantsa carnivorous plants. The yellow pitcher plant is common in wet pine savannas of Species Structure Pmax PNUE Refs –1 –1 µ –1 –1 (nmol CO2 g s )(mol CO2 mol N s ) the southeastern USA (Ref. 53). Its rosettes grow vegetatively and flower in multiple years beginning in Leaves 69.30 45.4 27 year three, and can persist for several decades. In these Pinguicula villosa Leaves 41.80 29.4 27 habitats, recurrent fires (with an average period of Leaves 56.70 37.7 27 three years) enhance the fecundity of S. alata and are Drosera rotundifolia Leaves 45.60 33.6 27 thought to be necessary for maintaining active Sarracenia purpurea Leaves 29.70 N.D. 26 population growth54. Brewer44 constructed a stage- vesiculosa Leaves 76.50 N.D 57 based matrix model of population growth and examined the consequences of altered fire frequency Bladders 23.62 N.D 31 on population growth rate. His analysis suggests that Utricularia macrorhiza Leaves 53.23 N.D 31 the finite rate of increase (λ), was higher for annually a Abbreviations: N, nitrogen, N.D., no data. burned populations (λ=1.104) than for populations

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burned at three-year intervals (λ=1.044) or for decades, and accumulating data have exposed the unburned populations (λ=1.028). Enhanced strengths and weaknesses of these models and recruitment in regularly burned populations shifts highlighted additional research needs. The primary the stable stage distribution towards smaller plants. data needed for refining these models are Distributions of reproductive value (the expected measurements across carnivorous taxa of number of offspring that will be produced by an photosynthetic rates as a function of nutrient individual of age x) are similar for annually burned availability; and photosynthetic capacity of populations and those burned at longer intervals. In noncarnivorous organs of carnivorous plants. both scenarios, transition probabilities for the Developmental variability in investment in persistence of juveniles and adults are the most carnivorous structures and sequestration of nutrients important contributors to λ. Infrequent fires might still for future growth or reproduction should be accounted be important because they suppress the development for in calculations of the efficiency of photosynthetic N of woody vegetation that can eventually shadow and use. These models do not account for ecological outcompete S. alata. Such demographic analyses could conflicts between prey capture and pollination, yet Acknowledgements We thank J.S. Brewer for a be applied profitably to other populations and species this conflict can affect not only evolutionary trends in preprint of his recent of carnivorous plants, especially those that are rare allocation to carnivorous organs, but also individual paper on Sarracenia alata and in need of intensive management. fitness and population dynamics. demography and A research approach that incorporates D.H. Benzing, E.J. Farnsworth, Conclusions and directions for future research reproductive effort and success, consequent J.S. Brewer and two Comparative and experimental studies at a wide population dynamics and clear measures of fitness anonymous reviewers for range of scales using unrelated organisms that share will illuminate the interplay of phylogenetic comments on this article. similar strong selective pressures can provide new constraints and evolutionary convergence in the Our research on carnivorous plants is insights into ecological processes and evolutionary evolutionary ecology of carnivorous plants. Because supported by the National dynamics. Carnivorous plants are exemplars for such carnivorous plants are threatened by overcollecting, Science Foundation studies, which have ranged from ecophysiology to and environmental change, the (DEB 98-05722 and DEB 98-08504) and the adaptive evolution. Cost–benefit models have results of such studies should guide conservation and Packard Foundation. provided a central focus for research for nearly two management strategies for these unique plants.

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Philip W. Hedrick

Genetic studies in endangered species have become widespread in the past Here, as an organizational theme for examining decade, and with new information from various genome projects, new the status and possible future of conservation applications and insights are forthcoming. Generally, neutral variants are used for genetics, I consider the three major types of genetic conservation applications, and when combined with highly variable loci and/or variation – NEUTRAL, DETRIMENTAL and ADAPTIVE many more markers, these approaches should become much more informative. (see Glossary) – and discuss how each is used in the Conservation genetics is also concerned with detrimental and adaptive variation, conservation of endangered species. Of course, which are more difficult to identify and characterize; however,the ability to whether a particular variant is neutral, detrimental predict the extent of such variation might become more successful and applied in or adaptive depends on the environment, population future conservation efforts. Neutral variants might be used to identify adaptive size, genetic background and so on. For example, a variants, but the overlay of different mutational processes and selective regimes particular allele that is adaptive, such as providing suggests that extreme caution should be used in making such identifications. resistance to an infectious disease in one environment, could be detrimental when the The recent extinction of many species, and continuing pathogen is absent because of a pleiotropic cost threats to many more has made conservation biology associated with that allele. Alternatively, genetic crucial in the 21st century. Although ecological, variants that are neutral in one situation could be political, economic, and other forces might be of adaptive in another. primary concern for avoiding the extinction of most I also consider one of the great promises of neutral endangered species, for long-term persistence, molecular variation, that of the use of the extent and genetics and related considerations has also been pattern of neutral variation to predict the amount Philip W. Hedrick a focus of conservation effort. In particular, the and significance of detrimental and adaptive Dept of Biology, Arizona application of new molecular techniques1 has made variation. Although it has not proven compelling in State University, Tempe, examination of genetics in endangered species some cases, with more informative loci and more AZ 85287, USA. e-mail: philip.hedrick@ feasible and genetic analysis has become widely genes, we might be able to utilize such observed asu.edu used in conservation research. associations better in the future.

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