Biological Conservation 153 (2012) 25–31 Contents lists available at SciVerse ScienceDirect Biological Conservation journal homepage: www.elsevier.com/locate/biocon Perspective Implications of different species concepts for conserving biodiversity Richard Frankham a,b,⇑, Jonathan D. Ballou c, Michele R. Dudash d, Mark D.B. Eldridge b, Charles B. Fenster d, Robert C. Lacy e, Joseph R. Mendelson III f,g, Ingrid J. Porton h, Katherine Ralls c, Oliver A. Ryder i a Department of Biological Sciences, Macquarie University, NSW 2109, Australia Australian Museum, 6 College Street, Sydney, NSW 2010, Australia c Center for Conservation and Evolutionary Genetics, Smithsonian Conservation Biology Institute, Washington, DC 20008, USA d Department of Biology, University of Maryland, College Park, MD 20742, USA e Chicago Zoological Society, Brookfield, IL 60513, USA f Zoo Atlanta, 800 Cherokee Ave., SE Atlanta, GA 30315, USA g School of Biology, Georgia Institute of Technology, 301 Ferst Dr, Atlanta, GA 30332, USA h Saint Louis Zoo, One Government Drive, St. Louis, MO 63110, USA i San Diego Zoo Institute for Conservation Research, 15600 San Pasqual Valley Road, Escondido, CA 92027, USA b a r t i c l e i n f o Article history: Received 16 January 2012 Received in revised form 17 April 2012 Accepted 28 April 2012 Available online 29 June 2012 Keywords: Fragmented populations Genetic rescue Inbreeding depression Loss of genetic diversity Outbreeding depression Species concepts a b s t r a c t The 26 definitions of species often yield different numbers of species and disparate groupings, with financial, legal, biological and conservation implications. Using conservation genetic considerations, we demonstrate that different species concepts have a critical bearing on our ability to conserve species. Many species of animals and plants persist as small isolated populations suffering inbreeding depression, loss of genetic diversity, and elevated extinction risks. Such small populations usually can be rescued by restoring gene flow, but substantial genetic drift effects can lead them to be classified as distinct species under the diagnostic phylogenetic species concept. Minimum harm to fitness is done and maximum potential fitness and evolutionary potential benefits accrue when reproductive isolation (pre- and/or post-zygotic) is used as the criterion to define distinct species. For sympatric populations, distinct species are diagnosed by very limited gene flow. For allopatric populations, both minimal gene flow and evidence of reduced reproductive fitness in crosses (or effects predicted from adaptive differentiation among populations and/or fixed chromosomal differences) are required to satisfy conservation issues. Species delineations based upon the biological and differential fitness species concepts meet the above requirements. Conversely, if species are delineated using the diagnostic phylogenetic species concept, genetic rescue of small genetically isolated populations may require crosses between species, with consequent legal and regulatory ramifications that could preclude actions to prevent extinction. Consequently, we conclude that the diagnostic phylogenetic species concept is unsuitable for use in conservation contexts, especially for classifying allopatric populations. Ó 2012 Elsevier Ltd. All rights reserved. Contents 1. 2. 3. 4. 5. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Minimizing harm and maximizing potential conservation benefits . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . How do excessively broad species delineations occur? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . How does excessive splitting of small populations occur? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Theory predicting generations to attain reciprocal monophyly or no shared alleles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Empirical data on rapid attainment of diagnosable differences between populations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26 26 27 28 28 29 30 Abbreviations: BSC, biological species concept; CE, critically endangered; E, endangered; ESC, evolutionary species concept; DFSC, differential fitness species concept; ID, inbreeding depression; OD, outbreeding depression; PSC, phylogenetic species concept; TSC, taxonomic species concept; V, vulnerable. ⇑ Corresponding author at: Department of Biological Sciences, Macquarie University, NSW 2109, Australia. Tel.: +61 2 9850 8186; fax: +61 2 9850 8245. E-mail addresses: richard.frankham@mq.edu.au (R. Frankham), ballouj@si.edu (J.D. Ballou), mdudash@umd.edu (M.R. Dudash), mark.eldridge@austmus.gov.au (M.D.B. Eldridge), cfenster@umd.edu (C.B. Fenster), rlacy@ix.netcom.com (R.C. Lacy), jmendelson@zooatlanta.org (J.R. Mendelson III), Porton@stlzoo.org (I.J. Porton), rallsk@thegrid.net (K. Ralls), oryder@sandiegozoo.org (O.A. Ryder). 0006-3207/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.biocon.2012.04.034 26 R. Frankham et al. / Biological Conservation 153 (2012) 25–31 6. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . . . Appendix A. Supplementary material References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction There are at least 26 definitions of biological species (see Wilkins, 2009; Hausdorf, 2011). Use of different species concepts to classify species has potential financial, legal, biological and conservation implications (Hey et al., 2003). It leads to much confusion and controversy, and to potential problems of inappropriate delineation of species for conservation purposes. Mace (2004) concluded that ‘taxonomists and conservationists need to work together to design some explicit rules to delimit the units included as species for the purposes of conservation planning and assessment.’ Thus, there is an urgent need to evaluate the suitability of the different species concepts for conservation purposes. The three concepts most widely used by the systematic and conservation communities are the biological species concept (BSC; Mayr, 1942, 1963), the evolutionary species concept (ESC; Simpson, 1951, 1961; Wiley, 1978) and the phylogenetic species concept (PSC; Eldredge and Cracraft, 1980; Cracraft, 1997), as defined in Table 1. We also discuss the recently proposed differential fitness species concept (DFSC; Hausdorf, 2011), as it is highly relevant to conservation. This concept is most similar to the BSC, but BSC uses mating isolation and/or sterility to delineate species while DFSC is broader, encompassing any pre- or post-zygotic fitness decrement following attempted crossing. An alternative to the use of defined species concepts is to rely upon the judgment of taxonomists, sometimes referred to as the taxonomic species concept (TSC; Mayden, 1997). This corresponds to the definition that species are ‘whatever a competent taxonomist chooses to call a species’ (Wilkins, 2009). This seems to be widely practised, as papers on new species delineations, or revisions usually fail to specify what species concept has been used (see McDade, 1995). As the literature on species concepts is massive, we can only refer to a sample of references. We favored key references, reviews, recent publications, and studies addressing conservation concerns. All of the commonly used species concepts suffer from incongruencies with biological reality (Hausdorf, 2011), namely: 1. ‘reproductive barriers are often semipermeable to gene flow’ (Hey and Pinho, 2012); 2. ‘species can differentiate despite ongoing inter-breeding’ (sympatric speciation; Papadopulos et al., 2011); 3. ‘parallel speciation can occur due to parallel adaptation or recurrent polyploidizations’, and 4. ‘uniparental organisms are actually organized in units that resemble species of biparental organisms’; In addition, we conclude that: 5. development of reproductive isolation between populations usually accompanies genetic adaption to different environments (via natural selection, as proposed by Darwin (1859)), and/or fixed chromosomal differences (reviewed by Frankham et al., 2011; Sexton et al., 2011; see Supplementary material). The incongruities indicate that no species concept is without problems. Points 1 and 2 cause severe difficulties for the BSC; furthermore, it does not apply to asexual organisms. For PSC, Points 1, 2 and 3 cause difficulties. Point 3 may cause difficulties for ESC, but . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 30 30 30 30 ESC copes with the other points. Point 5 partly counters some of the problems, as it makes it feasible to predict reproductive isolations for diagnosing species under BSC and DFSC (see below) (Frankham et al., 2011). A serious concern with PSC is that technological advances (e.g. those lessening DNA sequencing costs) and increased effort lead to increased resolution among lineages, such that even individuals within populations can be diagnosably different (Avise and Ball, 1990; Groves, 2004; Winkler, 2010). Despite the disparate definitions, species concepts typically indicate that species are cohesive clusters of individuals that have at least partially different evolutionary paths representing different lineages (see Avise and Ball, 1990; Knowlton and Weigt, 1997; de Queiroz, 1998; Hey et al., 2003; Coyne and Orr, 2004; Hausdorf, 2011). The differences among concepts are typically in how far evolutionary population differentiation needs to proceed before the populations should be considered distinct species. All serious concepts recognise that populations inherently incapable of gene exchange are distinct species, while those exhibiting random mating in sympatry are conspecific. However, there are major differences in the treatment of partly diverged allopatric populations capable of gene flow without adverse fitness consequences, or with beneficial consequences. In allopatric populations, especially those with small population sizes, genetic drift and mutation will lead to diagnosably different units that are not intrinsically reproductively isolated (see below) that may be ephemeral under natural patterns of population separation and re-connection. Defining such units as species for conservation purposes may accelerate extinction of broader BSC species rather than preserve adaptive differences (see below). Scientists working in different disciplines or on disparate major taxa often favor alternative species concepts (Claridge et al., 1997). For example, evolutionary geneticists generally favor BSC (see Noor, 2002; Coyne and Orr, 2004) because it relates to the fitness consequences of gene flow between populations and the process of speciation. In contrast, some taxonomists now favor PSC (Cracraft, 1997; Groves, 2004), because it is considered easier to implement. Use of PSC results in more splitting: it yielded 49% more species than BSC on the same group of organisms (Agapow et al., 2004). In some cases, the groupings according to BSC and PSC were discordant, with PSC species not nested within BSC species, or vice versa. Such inconsistencies can often lead to different management, some resulting in adverse consequences for conservation of biodiversity. We evaluate methods for defining species from the perspective of conservation biology, advocating that definitions used in conservation biology should maximize conservation benefits. We show, from a population genetics perspective, that current methods for species’ delineation often lead to species’ classification that is too narrow, or too broad, both of which can compromise the conservation of the taxon’s biodiversity. We then recommend use of concepts that are most beneficial for conserving global biodiversity. 2. Minimizing harm and maximizing potential conservation benefits The ideal species concept for conservation purposes would minimize potential harm and maximize potential benefits, as measured by reproductive fitness and sustaining adaptive evolutionary processes. Loss and fragmentation of habitat stem- 27 R. Frankham et al. / Biological Conservation 153 (2012) 25–31 Table 1 Species definition according to different species concepts. Species concept Species definition Reference Biological (BSC) ‘Groups of actually or potentially interbreeding natural populations, which are reproductively isolated from other such groups’ Evolutionary (ESC) ‘A species is a lineage of ancestral descent which maintains its identity from other such lineages and which has its own evolutionary tendencies and historical fate’ ‘A species is the smallest diagnosable cluster of individual organisms within which there is a parental pattern of ancestry and descent’ ‘Species can be defined as groups of individuals that are reciprocally characterized by features that would have negative fitness effects in other groups and that cannot be regularly exchanged between groups upon contact’ Mayr (1942) Wiley (1978) Cracraft (1983) Hausdorf (2011) Phylogenetic (PSC) (diagnostic) Differential fitness (DFSC) ming from human population growth is one of the most severe threats to biodiversity (Millennium Ecosystem Assessment, 2005). Fragmentation of populations that were once widely distributed results in small, isolated populations potentially subject to loss of genetic diversity, inbreeding depression and increased risk of extinction (see Allendorf and Luikart, 2006; Frankham et al., 2010). Conservation of these populations often requires reestablishment of gene flow between them (Frankham et al., 2010). Further, it has been proposed that populations be translocated into new habitats to cope with global climate change. For populations with low genetic diversity, the best strategy is often to translocate admixed populations into new habitat (Weeks et al., 2011). Managers that advocate either the transfer of organisms between fragmented populations or restriction of such transfers need to consider the potential impacts of both outbreeding depression (OD – defined to include any deleterious consequences of crossing on mating preference, pre- or post-zygotic reproductive fitness), and inbreeding depression (ID – defined as the relative reduction of fitness in offspring of related mates compared to matings between unrelated individuals). Thus, definitions and delineations for taxa with fragmented populations should lead to units that simultaneously (a) minimize OD, whilst (b) allowing maximum opportunities to outcross small inbred populations with low genetic diversity to reverse inbreeding depression and loss of genetic diversity (genetic rescue) (Frankham et al., 2010, 2011). The consequences of different species delineations for six hypothetical populations are illustrated in Fig. 1. Too broad a delineation of species in case 1 leads to a high risk of OD when populations a and b are crossed. Over splitting in case 2, as a result Populations Case a1 a2 a3 a4 of large genetic drift effects in small populations (see below), classifies the small a4 population as a distinct species, without any populations within its species that can be used to rescue it genetically or reinforce it demographically. This means that splitting, sometimes in an attempt to promote greater conservation of biodiversity, can actually prevent conservation actions necessary to preserve taxa with a small population size, and thereby result in greater loss of existing biodiversity. In case 3, use of reproductive isolation (defined as any adverse effect on pre-zygotic or post-zygotic fitness and equivalent to outbreeding depression) to delineate species a versus species b both minimizes the risk of outbreeding depression, and allows genetic rescue of small populations within species. Thus, to minimize harm and maximize benefits, species definitions and delineations need to define and identify populations that have or have not yet become reproductively isolated to a substantial degree. A possible approach to defining ‘‘substantial degree’’ is to compare the degree of reproductive isolation with that for well researched and widely accepted BSC species. Reluctance to test reproductive isolation may exacerbate the difficult process of implementing managed gene flow. We did not attempt to address definitions of units within species (e.g. sub-species and evolutionarily significant units) due to space constraints. 3. How do excessively broad species delineations occur? Excessively broad species delineations arise primarily from the use of characters (mainly morphological) with insufficient resolving power to delimit cryptic species. For example, the endangered grassland daisy Rutidosis leptorrhynchoides has been found to con- b1 b2 Species delineations Consequences of crossing 1 a1 a2 a3 a4 b1 b2 OD in a x b crosses 2 a1 a2 a3 a4 b1 b2 ID in a4 and no rescue, no OD 3 a1 a2 a3 a4 b1 b2 No OD and rescue of a4 possible Fig. 1. Consequences of crossing populations following different species delineations in relation to outbreeding depression (OD), inbreeding depression (ID) and genetic rescue. Populations a and b are reproductively isolated (show OD on crossing), but populations within them do not show reproductive isolation. The a4 population has a small effective population size, is inbred and has low genetic diversity. 28 R. Frankham et al. / Biological Conservation 153 (2012) 25–31 sist of diploid, tetraploid and hexaploid forms that are highly sterile upon crossing (Murray and Young, 2001). Further, well studied African elephants have recently been separated into savannah and forest species despite regions of contact, based upon genome wide deep sequence divergence between the two forms (Rohland et al., 2010). A second cause of excessive lumping occurs when speciation occurs in the face of gene flow, as may occur when strong adaptive differences drive reproductive isolation in sympatry. For example, Papadopulos et al. (2011) described 13 potential instances of speciation with gene flow for plants on Lord Howe Island, Australia. Use of neutral genetic markers (or organelle DNA) may result in such populations lacking fixed differences or reciprocal monophyly being classified as a single species under PSC, ESC or the BSC. Third, populations that diverged in allopatry may later come into contact and form hybrid zones with some introgression of alleles in each direction. If such populations do not show reciprocal monophyly or fixed differences they may be classified as a single species (Eldridge and Close, 1992). For example, several rock wallaby species in Australia that exhibit hybrid zones and lack reciprocal monophyly for mtDNA and allozymes were the subject of conflicting taxonomic delineations. Combined evidence from mtDNA, allozymes and chromosomes eventually led to resolution of their taxonomy, largely following chromosomal discontinuities (Eldridge and Close, 1992). 4. How does excessive splitting of small populations occur? Small isolated populations of conservation concern are subject to large genetic drift effects that can quickly result in genetic differentiation, without adaptation to different environments or the evolution of reproductive isolation. Further, fragmented populations that are now geographically isolated (allopatric), but not reproductively isolated may later come into contact and merge, as has happened many times in nature through environmental change (especially expansion and retreat of glaciers). For example, many mammal, bird, fish, lizard and plant species in Australia, Europe and the Americas show evidence of the merging of previously isolated and differentiated populations following climatic cycles (see Frankham et al., 2011 Supporting information). From a conservation perspective, such small populations are susceptible to being classified as different species according to the diagnostic version of PSC, especially when maternally inherited markers (mtDNA and cpDNA) and/or highly mutable genetic markers (microsatellites and animal mtDNA) are used in delineations. Relying on neutral markers is also problematic since they have been shown to be poor predictors of reproductive isolation, compared to adaptive differentiation in a diverse array of taxa (Nosil et al., 2002; Zigler et al., 2005; Stelkens and Seehausen, 2009; Thorpe et al., 2010; Wang and Summers, 2010). Below we discuss theory and empirical observations bearing on the problem of excessive splitting of small threatened populations. 4.1. Theory predicting generations to attain reciprocal monophyly or no shared alleles The issue of diagnosability under PSC has as its purpose to delineate populations where gene flow has ceased through either intrinsic (e.g. failure to mate, or F1 sterility) or extrinsic factors (e.g. geographic isolation, rivers, and mountains). Fixed gene differences (populations homozygous for different alleles) and reciprocal monophyly are required under different implementations of the diagnostic PSC (Cracraft, 1997; Groves, 2004; see Supplementary material). Lack of shared alleles between populations at one or more loci is sufficient to diagnose clusters that have experienced a long history without gene flow (see Supplementary material). Fixed gene differences are one form of unshared alleles, but more stringent than necessary to delineate lack of gene flow with multiple alleles. Confusingly, different authors use diverse definitions for fixed gene differences (see Supplementary material). The relevant theory on generations required for populations to be diagnosably different is couched in terms of reciprocal monophyly, no shared alleles or fixed gene differences. We present the first two estimates in the main text and the third in the Supplementary material, as the theoretical studies consider different scenarios, often with different assumptions. For reciprocal monophyly, it takes about 4Ne generations from the time that two populations separate for there to be a high probability of their having reciprocally monophyletic alleles for mtDNA (Niegel and Avise, 1986; Moritz, 1994; Hudson and Coyne, 2002), where Ne is the effective population size (defined in the Supplementary material; Frankham et al., 2010). Since the Ne for autosomal nuclear loci is four times that for mtDNA loci under the conditions of the models, it takes approximately 16Ne generations to attain reciprocal monophyly for nuclear autosomal loci (Hudson and Coyne, 2002). The probability of shared alleles/haplotypes for DNA sequences at a neutral nuclear autosomal locus approaches zero for divergence times greater than 10Ne generations (Hey, 1991; Supplementary material), and by extension 2.5Ne generations for mtDNA. The number of generations is also partially dependent upon allele frequencies in the common ancestral population (Kimura and Ohta, 1971). The number of generations to diagnosability will be less if multiple independent (unlinked) nuclear autosomal loci are genotyped (Hudson and Coyne, 2002). For example, if the probabilities that two populations are diagnosably different at each locus are all 0.5 (at the tth generation), then with 1, 2, 3 and 10 loci the probabilities of diagnosing populations as different are 0.5, 0.75, 0.875 and 0.999, respectively. Since we have a conservation focus, we ask how long it takes for reciprocal monophyly or no shared alleles to be detectable for threatened species (Table 2). For species with stable population sizes, the critically endangered (CE) IUCN (World Conservation Union, 2011) Red List category criterion D is defined by an adult census population size for the entire species (N)
Purchase answer to see full attachment