Implications of different species concepts for conserving biodiversity

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.

[1]  M. Noor Is the biological species concept showing its age , 2002 .

[2]  K. Summers,et al.  Genetic structure is correlated with phenotypic divergence rather than geographic isolation in the highly polymorphic strawberry poison‐dart frog , 2010, Molecular ecology.

[3]  John Alroy,et al.  Principles of genealogical concordance in species concepts and biological taxonomy , 1990 .

[4]  K. Queiroz**,et al.  The General Lineage Concept of Species, Species Criteria, and the Process of Speciation , 1998 .

[5]  R. Frankham,et al.  Introduction to Conservation Genetics , 2002 .

[6]  F. Palstra,et al.  Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? , 2008, Molecular ecology.

[7]  Michael J. Behe,et al.  Species: A History of the Idea , 2011 .

[8]  Georgina M Mace,et al.  The role of taxonomy in species conservation. , 2004, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[9]  A. Coleman Is there a molecular key to the level of "biological species" in eukaryotes? A DNA guide. , 2009, Molecular phylogenetics and evolution.

[10]  N. Knowlton,et al.  Species of marine invertebrates: a comparison of the biological and phylogenetic species concepts , 1997 .

[11]  B. Hausdorf PROGRESS TOWARD A GENERAL SPECIES CONCEPT , 2011, Evolution; international journal of organic evolution.

[12]  N. Baeshen,et al.  Biological Identifications Through DNA Barcodes , 2012 .

[13]  C. Darwin On the Origin of Species by Means of Natural Selection: Or, The Preservation of Favoured Races in the Struggle for Life , 2019 .

[14]  S. O’Brien,et al.  Bureaucratic mischief: recognizing endangered species and subspecies. , 1991, Science.

[15]  L. McDade Species concepts and problems in practice: insight from botanical monographs , 1995 .

[16]  E. Mayr Animal Species and Evolution , 1964 .

[17]  Y. Surget-Groba,et al.  Genetic Tests for Ecological and Allopatric Speciation in Anoles on an Island Archipelago , 2010, PLoS genetics.

[18]  Michele R. Dudash,et al.  Predicting the Probability of Outbreeding Depression , 2011, Conservation biology : the journal of the Society for Conservation Biology.

[19]  A. Wilson,et al.  Taxonomy of rock-wallabies, Petrogale (Marsupialia: Macropodidae). III. Molecular data confirms the species status of the purple-necked rock-wallaby (Petrogale purpureicollis Le Souef) , 2001 .

[20]  王丽华,et al.  国际生命条形码计划—DNA Barcoding , 2009 .

[21]  D. R. Robertson,et al.  How many species of goliath grouper are there? Cryptic genetic divergence in a threatened marine fish and the resurrection of a geopolitical species. , 2009 .

[22]  D. Biggs,et al.  Got Hybridization? A Multidisciplinary Approach for Informing Science Policy , 2010 .

[23]  E. Mayr Systematics and the Origin of Species , 1942 .

[24]  R. Nichols,et al.  Conservation biology: ‘Ghost’ alleles of the Mauritius kestrel , 2000, Nature.

[25]  R. Frankham Effective population size/adult population size ratios in wildlife: a review. , 1995, Genetical research.

[26]  C. Groves The What, Why and How of Primate Taxonomy , 2004, International Journal of Primatology.

[27]  H. Dawah,et al.  Species :the units of biodiversity , 1997 .

[28]  C. Moritz Defining 'Evolutionarily Significant Units' for conservation. , 1994, Trends in ecology & evolution.

[29]  O. Seehausen,et al.  Phenotypic divergence but not genetic distance predicts assortative mating among species of a cichlid fish radiation , 2009, Journal of evolutionary biology.

[30]  George Gaylord Simpson,et al.  Principles of Animal Taxonomy , 1961 .

[31]  D. Falconer,et al.  Introduction to Quantitative Genetics. , 1962 .

[32]  J. Hey,et al.  The structure of genealogies and the distribution of fixed differences between DNA sequence samples from natural populations. , 1991, Genetics.

[33]  D. Lambert,et al.  Is the black robin in genetic peril? , 1997 .

[34]  J. Ragle,et al.  IUCN Red List of Threatened Species , 2010 .

[35]  Andrew P Hendry,et al.  The speed of ecological speciation. , 2007, Functional ecology.

[36]  A. Young,et al.  Widespread Chromosome Variation in the Endangered Grassland Forb Rutidosis leptorrhynchoides F. Muell. (Asteraceae: Gnaphalieae) , 2001 .

[37]  K. Winker Is it a species , 2010 .

[38]  Stephen Cameron,et al.  A genomic perspective on the shortcomings of mitochondrial DNA for "barcoding" identification. , 2006, The Journal of heredity.

[39]  J. L. Gittleman,et al.  The Impact of Species Concept on Biodiversity Studies , 2004, The Quarterly Review of Biology.

[40]  B. Crespi,et al.  Host-plant adaptation drives the parallel evolution of reproductive isolation , 2002, Nature.

[41]  R. 19 A hierarchy of species concepts : the denouement in the saga of the species problem , 2009 .

[42]  R. Hudson,et al.  MATHEMATICAL CONSEQUENCES OF THE GENEALOGICAL SPECIES CONCEPT , 2002, Evolution; international journal of organic evolution.

[43]  The species concept. , 1949, Evolution; international journal of organic evolution.

[44]  G. Luikart,et al.  Conservation and the genetics of populations , 2006 .

[45]  R. Frankham,et al.  Introduction to conservation genetics, second edition , 2010 .

[46]  E. Wiley,et al.  The Evolutionary Species Concept Reconsidered , 1978 .

[47]  SEA URCHIN BINDIN DIVERGENCE PREDICTS GAMETE COMPATIBILITY , 2005, Evolution; international journal of organic evolution.

[48]  D. Briscoe,et al.  Allozyme evidence for extensive and ancient radiations in Australian Onychophora , 1995 .

[49]  R. Close,et al.  Fertile hybrids in two genera of wallabies: Petrogale and Thylogale. , 1997, The Journal of heredity.

[50]  R. Frankham,et al.  Rapid genetic deterioration in captive populations: Causes and conservation implications , 2002, Conservation Genetics.

[51]  R. Scholes,et al.  Ecosystems and human well-being: current state and trends , 2005 .

[52]  R. Frankham How closely does genetic diversity in finite populations conform to predictions of neutral theory? Large deficits in regions of low recombination , 2011, Heredity.

[53]  J. Hey,et al.  POPULATION GENETICS AND OBJECTIVITY IN SPECIES DIAGNOSIS , 2012, Evolution; international journal of organic evolution.

[54]  Swapan Mallick,et al.  Genomic DNA Sequences from Mastodon and Woolly Mammoth Reveal Deep Speciation of Forest and Savanna Elephants , 2010, PLoS biology.

[55]  T. Ohta,et al.  Theoretical aspects of population genetics. , 1972, Monographs in population biology.

[56]  L. Pope,et al.  Unprecedented Low Levels of Genetic Variation and Inbreeding Depression in an Island Population of the Black‐Footed Rock‐Wallaby , 1999 .

[57]  Joel Cracraft,et al.  Species Concepts and Speciation Analysis , 1983 .

[58]  Niles Eldredge,et al.  Phylogenetic Patterns and the Evolutionary Process. , 1981 .

[59]  R. Frankham,et al.  Assessing the benefits and risks of translocations in changing environments: a genetic perspective , 2011, Evolutionary applications.

[60]  Joanna Isobel House,et al.  Ecosystems and Human Wellbeing: Current State and Trends: Findings of the Conditions and Trend Working Group of the Millennium Ecosystem Assessment , 2006 .

[61]  John C. Avise,et al.  PHYLOGENETIC RELATIONSHIPS OF MITOCHONDRIAL DNA UNDER VARIOUS DEMOGRAPHIC MODELS OF SPECIATION , 1986 .

[62]  G. A. Horridge,et al.  Animal species and evolution. , 1964 .

[63]  Alexander S. T. Papadopulos,et al.  Speciation with gene flow on Lord Howe Island , 2011, Proceedings of the National Academy of Sciences.

[64]  Jody Hey,et al.  Understanding and confronting species uncertainty in biology and conservation , 2003 .

[65]  .. Cracraft Species concepts in systematics and conservation biology-an ornithological viewpoint ] , 2008 .

[66]  S. Strauss,et al.  Gene flow increases fitness at the warm edge of a species’ range , 2011, Proceedings of the National Academy of Sciences.

[67]  M. Eldridge,et al.  Taxonomy of Rock Wallabies, Petrogale (Marsupialia, Macropodidae) .1. A Revision of the Eastern Petrogale With the Description of 3 New Species , 1992 .

[68]  Michael C Whitlock,et al.  The incomplete natural history of mitochondria , 2004, Molecular ecology.

[69]  W. Atchley,et al.  Gene trees and the origins of inbred strains of mice. , 1991, Science.

[70]  B. Bowen,et al.  Evolutionary Significant Units versus Geopolitical Taxonomy: Molecular Systematics of an Endangered Sea Turtle (genus Chelonia) , 1999 .