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Bayesian phylogeny of Frankliniella schultzei COI haplotypes demonstrating the evolutionary relationship between the three colour morphs in Australia. Posterior probabilities exceeding 0.95 are indicated above each node. Representatives of other Frankliniella species for which COI sequence is available on GenBank are included under outgroups. Each Australian clade is illustrated with a photograph, either of a yellow, brown or black F. schultzei thrips (top to bottom respectively)
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Understanding and interpreting the host plant interactions of “generalist” herbivorous insects requires that species limits are accurately defined, as such taxa frequently harbour cryptic species with restricted host use. We tested for the presence of cryptic species across different host plant species in Australian Frankliniella schultzei using a...
Citations
... The ITS2 seq uences of the three F. xanthaner specimens with the COI sequences (GenBank accessions ON970365-ON970367), and several others (GenBank accessions ON986292-ON986298), harbored a single nucleotide indel and 6 further nucleotide substitutions. Further sampling may reveal that F. bruneri and F. xanthaner are in fact a complex of cryptic species similar to that found in F. occidentalis (Rugman-Jones et al. 2010) and F. schultzei (Hereward et al. 2017, Tyagi et al. 2017). ...
... DNA sequencing is a powerful tool that can facilitate the recognition of thrips species that are morphologically inseparable (cryptic species) or confirm morphological variation as either intra-or interspecific (Rugman-Jones et al. 2010, Gikonyo et al. 2017, Hereward et al. 2017, Tyagi et al. 2017. The most familiar application of DNA sequences for the purpose of species identification was introduced almost two decades ago and is referred to as "DNA barcoding" (Hebert et al. 2003a(Hebert et al. , 2003b. ...
No comprehensive identification resource is available for the genus Frankliniella. In response, a dynamic internet–based platform with interactive identification tools, species fact sheets and slide preparation tutorials are being developed by the author(s). We reviewed certain type, port interceptions, and origin collected specimens. We attempted to validate species identification using non-destructive DNA extraction and sequencing of both intercepted and field collected specimens. Sequences explicitly linked to a permanently curated morphological voucher specimen were deposited in a public repository (GenBank). The morphological review and genetic analysis revealed that both F. bruneri Watson and F. xanthaner Hood are each likely cryptic species complexes. Five species are described, F. ecuatoriana new species, F. funderburki new species, F. pelucensis new species, F. sanabriana new species and F. suramericana new species. Sequence data are recorded for the holotype specimens of the latter four species. Taxonomic status changes for F. genuina Hood and F. venusta Moulton are provided.
... Understanding the species status of natural enemies is an important step in selecting biological control agents (Gaskin et al., 2011;McCulloch et al., 2018;McCulloch et al., 2022;Rauth et al., 2011). For instance, genetic screening (typically with the mitochondrial COI gene) can uncover potential cryptic species (see Paterson et al., 2016;Smith et al., 2018), though additional genetic screening (typically with nuclear markers) is often required to confirm species status (Hereward et al., 2017;McCulloch et al., 2022;Toon et al., 2016). Furthermore, it has been suggested that sourcing biological control agents from the exact provenance of the invasive weed may be important (Gaskin et al., 2011;Goolsby et al., 2006), although this hypothesis requires further testing (see McCulloch et al., 2022). ...
... Furthermore, we recommend additional sampling in potential regions of overlap between the moth lineages (for example in Indonesia) to test their species status explicitly. If two of the C. exotica mitochondrial lineages have overlapping distributions, this will allow researchers to assess evidence of gene flow across the lineages, and test whether they represent distinct species (see Hereward et al., 2017;McCulloch et al., 2022;Toon et al., 2016). Ideally, gene flow should be assessed using nuclear markers, such as microsatellites or genome-wide SNPs (McCulloch et al., 2022). ...
... The extent of this overlap should be assessed further, by conducting additional sampling where these two mitochondrial lineages are found in sympatry in FNQ (Boggy Creek, Lilly Creek, Mareeba, and Riffle Creek) and the NT (Adelaide River and near Darwin at Fisherman's Wharf sites). Furthermore, specimens from the two lineages in the region of overlap should be tested for gene flow between them with population genetics methods (such as genotyping-by-sequencing or microsatellite markers), to assess their species status accurately (see Toon et al. 2016, Hereward et al. 2017. The overlapping distribution of these lineages means researchers must be particularly careful when collecting samples for host-testing (or subsequent field-release), to ensure that the correct mitochondrial lineage is sampled (at least until their species status has been assessed in a suitably designed test). ...
Acacia auriculiformis is a native Australian tree that has now become a category 1 invasive weed in Florida, USA. Previous research has identified Macrobathra moths as potential biological control agents for this weed, but little is known about the genetic diversity and structuring of these moths. In this study, we compared the genetic structure of four common Macrobathra moth species across the geographic distribution of A. auriculiformis –
and across regions where A. auriculiformis does not occur – to assess whether any of these moth species may comprise unrecognised cryptic species. We found contrasting patterns of genetic structuring among the four moth species, indicating that host-specific cryptic species could be present in Macrobathra arrectella and M. diplochrysa. Furthermore, we identified a deep genetic disjunction in both M. arrectella and M. callipetala across the Gulf of Carpentaria, a pattern that is also found in A. auriculiformis. The geographic distribution and host plant associations of the distinct mitochondrial lineages of each of these moth species should be further evaluated with additional ecological sampling, and the species status of these lineages tested directly, using additional molecular screening and/or carefully designed cross-mating tests.
... Many species of thrips are serious pests in a wide range of plants with economic importance, causing damage to them either directly through feeding, or indirectly by the transmission of orthotospoviruses [26][27][28]. Most of the pest thrips species belong to the family Thripidae [27], a taxon with more than 2000 species [29]; however, recent studies showed that many of these important thrips pest species are likely a complex of cryptic species, including Frankliniella occidentalis (Pergande) [30], Scirtothrips aurantii (Faure) [8], Scirtothrips dorsalis Hood [31], Frankliniella schultzei Trybom [32] and Thrips palmi Karny [33]. ...
Thrips tabaci Lindeman is a serious pest of various cultivated plants, with three, distinct lineages within a cryptic species complex. Despite the well-known significance of this pest, many attributes of these lineages are not yet fully understood, including their reproductive behaviour. We performed no-choice-design cross-mating experiments under a controlled laboratory environment with virgin adult individuals from all three lineages. The behaviour of thrips was recorded with a camera mounted on a stereomicroscope, and the recordings were analysed in detail. We found that the so-called leek-associated lineages of this cryptic species complex are reproductively isolated from the tobacco-associated lineage; therefore, they represent different species. Divergence in the behaviour of conspecific and heterospecific pairs became evident only after contact. There were no marked differences between the lineages in their precopulatory and copulatory behaviour, except in the duration of the latter. We confirmed mating between thelytokous females and arrhenotokous males; however, we assume some form of loss of function in the sexual traits of asexual females. The post-mating behaviour of males indicated the presence and role of an anti-aphrodisiac pheromone. We also demonstrated differences between lineages regarding their activity and their propensity for exhibiting an escape response upon interaction with heterospecific thrips.
... Conversely, mitochondrial markers often reveal significant genetic diversity within an arthropod species. Without supplementing the results from these markers with nuclear markers, however, it is not possible to test whether this diversity simply represents intraspecific variation, or whether a described species is instead composed of several cryptic species Toon et al., 2016;Hereward et al., 2017;Rafter and Walter, 2020). ...
... This sampling and screening should initially be used to delimit the geographic distribution of these divergent lineages, for this influences how the species status of these lineages may be assessed. If divergent mitochondrial lineages are in sympatry the species status of lineages can be assessed by screening nuclear markers to assess whether gene flow takes place across lineages through random mating Toon et al., 2016;Hereward et al., 2017). If populations that represent different lineages are in allopatry, their species status is most appropriately tested by functional analysis of their mating systems, to establish the responses of individuals from one population to individuals of the other allopatric population. ...
Biological control is often the most cost effective and environmentally sound method of managing widespread environmental weeds. Earlier detection of cryptic species and improved understanding of host-herbivore associations during the initial screening for effective natural enemies should further boost success rates. We formalise a framework for improved prioritisation of biological control agents through the successive feedback between ecological surveys and molecular screening. Incorporating enhanced molecular methods to strengthen hypothesis testing in the initial phases of exploratory research will help prioritise herbivores and regions for subsequent native range surveys, and should more readily uncover unrecognised cryptic species that may otherwise remain hidden. We postulate that this iterative methodology should enhance the environmental safety and cost-benefit ratios of future biological control programs, and this approach should help to elucidate problematic aspects of existing programs.
... For example, F. gemina cannot be distinguished satisfactorily from F. zucchini [41], despite them both being considered Orthotospovirus vectors. Even greater confusion exists with the worldwide pest, F. schultzei, within which molecular studies have distinguished a complex of sibling species [42]. However, no evidence has been produced of any consistent biological differences between these siblings, including their ability to transmit Orthotospoviruses. ...
Almost all of the thrips species that are considered pests are members of a single subfamily of Thripidae, the Thripinae, a group that represents less than 30% of the species in the insect Order Thysanoptera. Three of the five major Families of Thysanoptera (Aeolothripidae, Heterothripidae, Melanthripidae) are not known to include any pest species. The Phlaeothripidae that includes more than 50% of the 6300 thrips species listed includes very few that are considered to be pests. Within
the Thripidae, the members of the three smaller subfamilies, Panchaetothripinae, Dendrothripinae and Sericothripinae, include remarkably few species that result in serious crop losses. It is only in the subfamily Thripinae, and particularly among species of the Frankliniella genus-group and the Thrips genus-group that the major thrips species are found, including all but one of the vectors of Orthotospovirus infections. It is argued that the concept of pest is a socio-economic problem, with the pest status of any particular species being dependent on geographical area, cultivation practices, and market expectations as much as the intrinsic biology of any thrips species.
... Barriers to interbreeding between the color morphs appear to exist [97]. In addition to these two color morphs, a brown color morph of F. schultzei has been reported from Australia [98]. Despite their differences in color, these thrips morphs are considered as one species due to similar morphological and ecological features. ...
... However, based on COI phylogeny, F. schultzei appears to be a species complex [50,99] with three deeply divergent clades corresponding to the three distinct color morphs [87]. The yellow, black, and brown morphs are considered as three different species [98]. Cryptic species IIIa1 corresponds to the dark form, and IIa1 is similar to the pale/yellow form. ...
... Cryptic species IIIa1 corresponds to the dark form, and IIa1 is similar to the pale/yellow form. The yellow form of F. schultzei has been identified as a separate species, F. sulphurea Schmutz [98]. The description of F. sulphurea within F. schultzei by the systematists may be due to the co-occurrence with the dark form of F. schultzei on the same hosts [96]. ...
Simple Summary: Thrips are important agricultural and forest pests. They cause damage by sucking plant sap and transmitting several plant viruses. Correct identification is the key for epidemiological studies and formulating appropriate management strategies. The application of molecular and electronic detection platforms has improved the morphological character-based diagnosis of thrips species. This article reviews research on molecular and automated identification of thrips species and discusses future research strategies for rapid and high throughput thrips diagnosis. Abstract: Thrips are insect pests of economically important agricultural, horticultural, and forest crops. They cause damage by sucking plant sap and by transmitting several tospoviruses, ilar-viruses, carmoviruses, sobemoviruses, and machlomoviruses. Accurate and timely identification is the key to successful management of thrips species. However, their small size, cryptic nature, presence of color and reproductive morphs, and intraspecies genetic variability make the identification of thrips species challenging. The use of molecular and electronic detection platforms has made thrips identification rapid, precise, sensitive, high throughput, and independent of developmental stages. Multi-locus phylogeny based on mitochondrial, nuclear, and other markers has resolved ambiguities in morphologically indistinguishable thrips species. Microsatellite, RFLP, RAPD, AFLP, and CAPS markers have helped to explain population structure, gene flow, and intraspecies heterogeneity. Recent techniques such as LAMP and RPA have been employed for sensitive and on-site identification of thrips. Artificial neural networks and high throughput diagnostics facilitate automated identification. This review also discusses the potential of pyrosequencing, microarrays, high throughput sequencing, and electronic sensors in delimiting thrips species.
... Nevertheless, further testing of their species status is warranted. The species status of these lineages could be assessed using additional molecular markers if they are found together in regions of sympatry (see Toon et al., 2016, Hereward et al., 2017, or through the investigation of their pheromones if the two species are entirely allopatric (Lassance et al., 2019). ...
Acacia auriculiformis is a native Australian tree that has developed into a damaging environmental weed in Florida, USA. We conducted field surveys to collect insect herbivores from A. auriculiformis and three closely related allopatric congeners (A. crassa, A. leiocalyx, and A. concurrens) across the native distribution of each plant species. We collected over 800 specimens, comprising a diversity of herbivorous insect groups, and successfully sequenced 480 specimens for DNA barcoding to group them into molecular operational taxonomic units (MOTUs) as a first step in documenting this diversity. Most herbivores (85%) were found on only a single Acacia species, suggesting each Acacia species hosts its own unique herbivore complex. The Northern Territory and Far North Queensland A. auriculiformis populations are allopatric in relation to one another but hosted a similar suite of herbivores. Calomela intemerata and seven lepidopteran species (including three species of Macrobathra moths) were particularly abundant across both regions. These herbivores look promising as potential biological control agents, though their host-specificity and genetic diversity should be investigated further.
... Some invasive insects, once seen as one generalist species, have been found to represent a complex of cryptic species, with each one relatively more specialized in its host use (Dumas et al., 2015;Malka et al., 2018;Rafter, Hereward, & Walter, 2013). But genetic analysis has also revealed cryptic species complexes comprised of different generalist species (Gikonyo et al., 2017;Hereward, Hutchinson, McCulloch, Silva, & Walter, 2017;Vyskočilová, Seal, & Colvin, 2019). All of this implies that close attention should be paid when divergent evolutionary lineages have already been documented in a particular species. ...
... Insects that exhibit differences in host use across their invasive and native ranges, as seen in S. aurantii (Rafter et al., 2013), provide a clear signal that more than one species may be involved. However, when considerable overlap is evident in host use across evolutionary lineages (Hereward et al., 2017;Vyskočilová et al., 2019), detecting the presence of cryptic species becomes more difficult (Paterson, 1991;Walter, 2003). This is particularly relevant to generalist insect herbivores because the diversity of their host interactions tends to obscure any differences across species. ...
... Climatic tolerances might be one important component of speciation for host-plant generalists more broadly (Brunner & Frey, 2010;Gikonyo et al., 2017;Hereward et al., 2017). In Australia, N. viridula from eastern regions experience much cooler conditions and more variable photoperiods than those in the north-western region (Table S8) (Musolin, Tougou, & Fujisaki, 2011;Tougou et al., 2009;Yukawa et al., 2007) and this pattern may, in part, be because European lineage bugs invaded that country. ...
The presence of distinct evolutionary lineages within herbivorous pest insect taxa requires close attention. Scientific understanding, biosecurity planning and practice, and pest management decision making each suffer when such situations remain poorly understood. The pest bug Nezara viridula Linnaeus has been recorded from numerous host plants and has two globally distributed mitochondrial (mtDNA) lineages. These mtDNA lineages co‐occur in few locations globally and the consequences of their divergence and recent secondary contact has not been assessed. We present evidence that both mtDNA lineages of N. viridula are present in Australia and their haplotype groups have a mostly separate distribution from one another. The north‐western population has only Asian mtDNA haplotypes, and the population with an eastern distribution is characterized mostly by European mtDNA haplotypes. Haplotypes of both lineages were detected together at only one site in the north of eastern Australia and microsatellite data indicate that this secondary contact has resulted in mating across the lineages. Admixture and the movement of mtDNA haplotypes outside of this limited area of overlap has not, however, been extensive. Some degree of mating incompatibility or differences in the climatic requirements and tolerances of the two lineages, and perhaps a combination of these influences, might limit introgression and the movement of individuals, but this needs to be tested. This work provides the foundation for further ecological investigation of the lineages of N. viridula, particularly the consequences of admixture on the ecology of this widespread pest. We propose that for now, the Asian and European lineages of N. viridula would best be investigated as subspecies, so that ‘pure’ and admixed populations of this bug can each be considered directly with respect to management and research priorities.
... The Recognition Concept of species is the most direct concept mechanistically because it focuses on how individual organisms meet and mate within their usual environmental context (e.g., Paterson 1991;Walter 2003;Rafter and Walter 2013a;Hereward et al. 2017). It thus provides the most realistic framework for testing for the possibility of cryptic species. ...
... Several technical approaches are available for investigating the possibility of cryptic species, with the technique of choice dictated (to a considerable extent) by the structure of the mating system of the organisms concerned, particularly the mode(s) of sexual signalling with which they communicate. They include observational analyses of mate recognition or characterisation of the Specific Mate Recognition System (SMRS) (Milne et al. 2002;Rafter and Walter 2013b;Rungrojwanich and Walter 2000;Walter 2003), reciprocal cross-mating tests on the recognition process (Fernando and Walter 1997;Milne et al. 2007;Rafter and Walter 2013b;Wongnikong et al. 2019) (both of which allow allopatric populations to be tested), and analyses of gene flow between host-associated populations in sympatry (Hereward et al. 2013b(Hereward et al. , 2017Rafter and Walter 2013a;McKendrick et al. 2017). Even asexual populations can be considered although it is their behaviour relative to their host plants that provides the focus for investigation, as with different host-associated cotton aphids that proved to be different species (Nagar-Rodriguez et al. 2009). ...
... O. nubilalis (Malausa et al. 2007;Martel et al. 2003), Enchenopa binotata Say (Hemiptera, Membracidae) (Guttman et al. 1981)), or a complex of both host-associated specialists and polyphagous species (e.g. Liriomyza trifolii Burgess (Diptera, Agromyzidae) (Scheffer and Lewis 2006), S. aurantii (Rafter et al. 2013), and F. schultzei (Hereward et al. 2017)). The mistaken inclusion of cryptic species under one name has the potential to confuse ecological interpretation considerably and, consequently, any applied ecology measures taken against the organisms in question (Paterson 1991;Walter 2003;Bickford et al. 2007). ...
Generalist insect herbivores, those recorded as using numerous hosts (tens or even hundreds of species), are not well understood ecologically. We suggest ways to investigate the ecology of these species beyond the practice of accumulating host records. We present reasons why multiple host use by herbivorous insects needs to be quantified in the field, both locally and geographically, and also through time. Further, the host use patterns generated must be based on certain knowledge that cryptic species are not conflated in the results as one species. Such results reveal a lot about the ecology of the species concerned and about generalist–host relationships more widely. This provides a sound basis for the functional significance of multiple host use to be interpreted and tested further. Structured sampling programs conducted previously in the field indicate that generalist insect herbivores are strongly associated with only a relatively small subset of their recorded host species, their primary host plants. A focus on these particular host plants is fundamental to (i) understanding the ecology of the herbivore species in question and (ii) investigating the sensory and behavioural mechanisms associated with host location. We conclude that the principal influence on patterns of multiple host use in the field is the mechanism by which herbivorous insects recognise cues from potential hosts and use them to localise plants. These mechanisms represent species-specific and species-wide adaptations to the usual environment of the species in question. Working from this perspective should contribute substantially to developing a strong and realistic interpretation of the origins and functional significance of multiple host use in herbivorous arthropods.
