The <i>Scirtothrips dorsalis</i> Species Complex: Endemism and Invasion in a Global Pest

<div><p>Invasive arthropods pose unique management challenges in various environments, the first of which is correct identification. This apparently mundane task is particularly difficult if multiple species are morphologically indistinguishable but accurate identification can be determined with DNA barcoding provided an adequate reference set is available. <i>Scirtothrips dorsalis</i> is a highly polyphagous plant pest with a rapidly expanding global distribution and this species, as currently recognized, may be comprised of cryptic species. Here we report the development of a comprehensive DNA barcode library for <i>S</i>. <i>dorsalis</i> and seven nuclear markers via next-generation sequencing for identification use within the complex. We also report the delimitation of nine cryptic species and two morphologically distinguishable species comprising the <i>S</i>. <i>dorsalis</i> species complex using histogram analysis of DNA barcodes, Bayesian phylogenetics, and the multi-species coalescent. One member of the complex, here designated the South Asia 1 cryptic species, is highly invasive, polyphagous, and likely the species implicated in tospovirus transmission. Two other species, South Asia 2, and East Asia 1 are also highly polyphagous and appear to be at an earlier stage of global invasion. The remaining members of the complex are regionally endemic, varying in their pest status and degree of polyphagy. In addition to patterns of invasion and endemism, our results provide a framework both for identifying members of the complex based on their DNA barcode, and for future species delimiting efforts.</p></div

Nucleotide diversity (<i>π</i>) for 33 populations of 6 species within the <i>Scirtothrips dorsalis</i> species complex (Table A of S1 File).

<p>Numbered populations correspond to <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.t004" target="_blank">Table 4</a>. Population 35 is <i>S</i>. <i>aff</i>. <i>dorsalis</i>.</p

Bayes factors favor partitioned over unpartitioned phylogenetic analyses.

<p>¹A Bayes factor of at least 10 is interpreted as significant favoring the more complex partitioned model after Kass & Raftery [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.ref070" target="_blank">70</a>].</p><p>Bayes factors favor partitioned over unpartitioned phylogenetic analyses.</p

South Asia 1 cryptic species portion of the <i>Scirtothrips dorsalis</i> COI gene tree (75% consensus) showing multiple invasive maternal lineages now present in Israel (orange/yellow), Japan (green), and South Asia, East Asia, and North America (purple, blue, brown).

<p>Support subtending each node is the posterior clade frequency out of 100. * denotes frequency in >99.9% of trees. A single member of the South Asia 2 cryptic species roots the tree. Includes DNA sequences from this study (Table A of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>) and those mined from GenBank (Table B of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>).</p

Population genetics parameters and tests.

<p>-Abbreviations: n-sample size, %C-frequency of common invasive haplotype.</p><p>-Descriptive statistics: π-nucleotide diversity, HD-haplotype diversity, τ-the date of population growth in mutational time under the expansion model, rg-raggedness, F*-Fu&Li’s F*, D*-Fu&Li’s D*, D-Tajima’s D, Fs-Fu’s Fs.</p><p>-Statistical tests: ND-probability of non-differentiation (used to justify combining India, Israel, and select invasive populations as panmictic), E_D-test of demographic expansion p-value, E_S-test of spatial expansion p-value.</p><p>-Descriptive statistics could not be calculated for populations with HD = 0.</p><p>-Expansion tests were conducted for panmictic populations and populations where n>7.</p><p>-Significance is assessed under a two-tailed test for all test statistics and ND and a one-tailed test for E_D and E_S.</p><p>-Bold denotes significance favoring expansion while italics denote significance rejecting an expansion model.</p><p>¹Farris <i>et al</i>. [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.ref012" target="_blank">12</a>];</p><p>²The invasive panmictic population includes all populations with a sample size >7 and a common invasive haplotype frequency >90%.</p><p>Population genetics parameters and tests.</p

Ranges of species within the <i>Scirtothrips dorsalis</i> complex.

<p>AU1- Australia 1, AU2- Australia 2, AU3- Australia 3, EA2- East Asia 2, EA3- East Asia 3, EA4- East Asia 4. Includes haplotypes detected in this study (white, Table A of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>) and mined from GenBank (yellow, Table B of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>). The earth global view used in this figure consists of MODIS satellite data for the NASA Blue Marble 2002 project. These images are freely available to educators, scientists, museums, and the public.</p

Important biological characteristics of species within the <i>S</i>. <i>dorsalis</i> complex.

<p>¹Host range is determined here based on DNA barcode records (Tables A-B of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>) or from [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.ref005" target="_blank">5</a>] for <i>S</i>. <i>oligochaetus</i> (Table B of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>) and is likely higher for many species within the complex.</p><p>²Pest status is determined here based on detection on at least one commercial host.</p><p>³Invasion potential is determined based on a “history of invasion” criterion [<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.ref023" target="_blank">23</a>]. This is inferred based on range maps (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.g003" target="_blank">Fig 3</a>) and the presence of low diversity (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.g005" target="_blank">Fig 5</a>) or newly detected populations at the periphery of ranges.</p><p>Important biological characteristics of species within the <i>S</i>. <i>dorsalis</i> complex.</p

Bayesian species-level phylogeny of the <i>Scirtothrips dorsalis</i> complex.

<p>Based on the consensus sequences of nine concatenated loci for each species and including DNA sequences from this study (Table A of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>) and those mined from GenBank (Table B of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0123747#pone.0123747.s003" target="_blank">S1 File</a>). Support subtending each node is the posterior clade frequency out of 100. * denotes frequency in >99.9% of trees.</p