Is phylogenetic relatedness to native species important for the establishment of reptiles introduced to California and Florida?

Aim  Charles Darwin posited that introduced species with close relatives were less likely to succeed because of fiercer competition resulting from their similarity to residents. There is much debate about the generality of this rule, and recent studies on plant and fish introductions have been inconclusive. Information on phylogenetic relatedness is potentially valuable for explaining invasion outcomes and could form part of screening protocols for minimizing future invasions. We provide the first test of this hypothesis for terrestrial vertebrates using two new molecular phylogenies for native and introduced reptiles for two regions with the best data on introduction histories. Location  California and Florida, USA. Methods  We performed an ordination of ecological traits to confirm that ecologically similar species are indeed closely related phylogenetically. We then inferred molecular phylogenies for introduced and native reptiles using sequence data for two nuclear and three mitochondrial genes. Using these phylogenies, we computed two distance metrics: the mean phylogenetic distance (MPD) between each introduced species and all native species in each region (which indicates the potential interactions between introduced species and all native species in the community) and the distance of each introduced species to its nearest native relative – NN (indicating the degree of similarity and associated likelihood of competition between each introduced species and its closest evolutionary analogue). These metrics were compared for introduced species that established and those that failed. Results  We demonstrate that phylogenetically related species do share similar ecological functions. Furthermore, successfully introduced species are more distantly related to natives (for NN and MPD) than failed species, although variation is high. Main conclusions  The evolutionary history of a region has value for explaining and predicting the outcome of human-driven introductions of reptiles. Phylogenetic metrics are thus useful inputs to multi-factor risk assessments, which are increasingly required for screening introduced species.

[1]  D. Simberloff The Role of Propagule Pressure in Biological Invasions , 2009 .

[2]  Craig R. Allen,et al.  Predictors of Introduction Success in the South Florida Avifauna , 2006, Biological Invasions.

[3]  M. Rejmánek A theory of seed plant invasiveness: The first sketch , 1996 .

[4]  D. Simberloff,et al.  BIOTIC INVASIONS: CAUSES, EPIDEMIOLOGY, GLOBAL CONSEQUENCES, AND CONTROL , 2000 .

[5]  T. Blackburn,et al.  The role of propagule pressure in explaining species invasions. , 2005, Trends in ecology & evolution.

[6]  J. Oliver,et al.  Establishment of the foreign partheonogenetic tick Amblyomma rotundatum (Acari: Ixodidae) in Florida. , 1993, The Journal of parasitology.

[7]  D. Richardson,et al.  Searching for phylogenetic pattern in biological invasions , 2007 .

[8]  D. Faith Conservation evaluation and phylogenetic diversity , 1992 .

[9]  S. Barry,et al.  Predicting establishment success for alien reptiles and amphibians: a role for climate matching , 2009, Biological Invasions.

[10]  L. Harmon,et al.  Competition and community structure in diurnal arboreal geckos (genus Phelsuma) in the indian Ocean , 2007 .

[11]  Jan Pergl,et al.  Geographical and taxonomic biases in invasion ecology. , 2008, Trends in ecology & evolution.

[12]  Craig R. Allen,et al.  Body Mass Patterns Predict Invasions and Extinctions in Transforming Landscapes , 1999, Ecosystems.

[13]  M Rejmánek,et al.  Plant invasions — the role of mutualisms , 2000, Biological reviews of the Cambridge Philosophical Society.

[14]  Richard P Duncan,et al.  Darwin's naturalization conundrum: dissecting taxonomic patterns of species invasions. , 2008, Ecology letters.

[15]  David M. Richardson,et al.  Conifers as invasive aliens: a global survey and predictive framework , 2004 .

[16]  M. Cadotte,et al.  Ecological Patterns and Biological Invasions: Using Regional Species Inventories in Macroecology , 2006, Biological Invasions.

[17]  L. Luiselli Food niche overlap between sympatric potential competitors increases with habitat alteration at different trophic levels in rain-forest reptiles (omnivorous tortoises and carnivorous vipers) , 2006, Journal of Tropical Ecology.

[18]  J. Felsenstein Phylogenies and the Comparative Method , 1985, The American Naturalist.

[19]  R. Duncan,et al.  Ecology: Darwin's naturalization hypothesis challenged , 2002, Nature.

[20]  Campbell O. Webb,et al.  Exotic taxa less related to native species are more invasive. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[21]  Campbell O. Webb,et al.  Bioinformatics Applications Note Phylocom: Software for the Analysis of Phylogenetic Community Structure and Trait Evolution , 2022 .

[22]  Mark Vellend,et al.  Conceptual Synthesis in Community Ecology , 2010, The Quarterly Review of Biology.

[23]  Petr Pyšek,et al.  Is there a taxonomic pattern to plant invasions , 1998 .

[24]  Campbell O. Webb,et al.  Exploring the Phylogenetic Structure of Ecological Communities: An Example for Rain Forest Trees , 2000, The American Naturalist.

[25]  D. Richardson,et al.  A Quantitative Climate-Match Score for Risk-Assessment Screening of Reptile and Amphibian Introductions , 2009, Environmental management.

[26]  E. Louis,et al.  Molecular phylogenetics of squamata: the position of snakes, amphisbaenians, and dibamids, and the root of the squamate tree. , 2004, Systematic biology.

[27]  J. Schulte,et al.  PHYLOGENETIC RELATIONSHIPS WITHIN IGUANIDAE INFERRED USING MOLECULAR AND MORPHOLOGICAL DATA AND A PHYLOGENETIC TAXONOMY OF IGUANIAN LIZARDS , 2003 .

[28]  Brendan A. Wintle,et al.  Alien invaders and reptile traders: what drives the live animal trade in South Africa? , 2010 .

[29]  A. Ricciardi,et al.  Does Darwin’s Naturalization Hypothesis Explain Fish Invasions? , 2006, Biological Invasions.

[30]  S. Kark,et al.  The role of species traits and taxonomic patterns in alien bird impacts , 2009 .

[31]  H. MacIsaac,et al.  Popularity and Propagule Pressure: Determinants of Introduction and Establishment of Aquarium Fish , 2006, Biological Invasions.

[32]  T. Fritts,et al.  THE ROLE OF INTRODUCED SPECIES IN THE DEGRADATION OF ISLAND ECOSYSTEMS: A Case History of Guam1 , 1998 .

[33]  W. Thuiller,et al.  Resolving Darwin’s naturalization conundrum: a quest for evidence , 2010 .

[34]  C. Daehler Darwin's Naturalization Hypothesis Revisited , 2001, The American Naturalist.

[35]  S. Allan,et al.  INTRODUCTION OF POTENTIAL HEARTWATER VECTORS AND OTHER EXOTIC TICKS INTO FLORIDA ON IMPORTED REPTILES , 2000, The Journal of parasitology.

[36]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[37]  T. A. Hall,et al.  BIOEDIT: A USER-FRIENDLY BIOLOGICAL SEQUENCE ALIGNMENT EDITOR AND ANALYSIS PROGRAM FOR WINDOWS 95/98/ NT , 1999 .

[38]  Effects of Sarcophagid Fly Infestations on Green Anole Lizards (Anolis carolinensis): An Analysis across Seasons and Age/Sex Classes , 2006 .

[39]  S. Hedges,et al.  The phylogeny of squamate reptiles (lizards, snakes, and amphisbaenians) inferred from nine nuclear protein-coding genes. , 2005, Comptes rendus biologies.

[40]  L. Meyerson,et al.  Saving camels from straws: how propagule pressure-based prevention policies can reduce the risk of biological invasion , 2008, Biological Invasions.