Phylogenomic and mitogenomic data can accelerate inventorying of tropical beetles during the current biodiversity crisis
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Evaluation Summary:
This manuscript provides some clear ideas on the use of next-generation sequencing data to rapidly increase biodiversity inventories and set the basis for future research. The principal objective of this study is to demonstrate how biodiversity information for a hyperdiverse tropical group can be rapidly expanded via targeted field research and large-scale sequencing. The authors use a comprehensive sampling for a tribe of beetles with complicated morphological characters, highlight the existence of multiple undescribed taxa. The database of sequences could set a benchmark for the spatiotemporal evaluation of biodiversity, would support evidence-based conservation planning, and would provide a robust framework for systematic, biogeographic, and evolutionary studies.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Abstract
Conservation efforts must be evidence-based, so rapid and economically feasible methods should be used to quantify diversity and distribution patterns. We have attempted to overcome current impediments to the gathering of biodiversity data by using integrative phylogenomic and three mtDNA fragment analyses. As a model, we sequenced the Metriorrhynchini beetle fauna, sampled from ~700 localities in three continents. The species-rich dataset included ~6500 terminals, ~ 1850 putative species delimited at 5% uncorrected pairwise threshold, possibly ~1000 of them unknown to science. Neither type of data could alone answer our questions on biodiversity and phylogeny. The phylogenomic backbone enabled the integrative delimitation of robustly defined natural genus-group units that will inform future research. Using constrained mtDNA analysis, we identified the spatial structure of species diversity, very high species-level endemism, and a biodiversity hotspot in New Guinea. We suggest that focused field research and subsequent laboratory and bioinformatic workflow steps would substantially accelerate the inventorying of any hyperdiverse tropical group with several thousand species. The outcome would be a scaffold for the incorporation of further data from environmental sequencing and ecological studies. The database of sequences could set a benchmark for the spatiotemporal evaluation of biodiversity, would support evidence-based conservation planning, and would provide a robust framework for systematic, biogeographic, and evolutionary studies.
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Author Response:
Reviewer #1:
In this manuscript, the authors make use of next-generation sequencing to provide a preliminary inventory of tribe Metriorrhynchini, a hyperdiverse group of beetles with intricate systematics mainly due to likely morphological convergence of their Millerian rings. The authors provide an admirable sampling within Africa, Asia and Oceania, with about 700 successfully sampled localities and thousands of specimens.
The main result of the manuscript is the curated database of Metriorrhynchini that will be useful in future research. In addition, different statistical methods are used to provide an idea of the undescribed species within the tribe, the astonishing species richness in New Guinea or the use of phylogenomic data to explore major phylogenetic relationships. However, some of the author's claims …
Author Response:
Reviewer #1:
In this manuscript, the authors make use of next-generation sequencing to provide a preliminary inventory of tribe Metriorrhynchini, a hyperdiverse group of beetles with intricate systematics mainly due to likely morphological convergence of their Millerian rings. The authors provide an admirable sampling within Africa, Asia and Oceania, with about 700 successfully sampled localities and thousands of specimens.
The main result of the manuscript is the curated database of Metriorrhynchini that will be useful in future research. In addition, different statistical methods are used to provide an idea of the undescribed species within the tribe, the astonishing species richness in New Guinea or the use of phylogenomic data to explore major phylogenetic relationships. However, some of the author's claims should be questioned:
- Surprisingly, the authors rely on a very low threshold to identify mOTUs (2% in the manuscript). The authors refer to Hebert et al. (2003) and Eberle et al. (2020) to justify the threshold, but still, they are likely overestimating the number of mOTUs and thus, considering putative species what it may be different populations. Figure S17 provide estimates of mOTUs with different thresholds (1 to 10%), which rapidly decrease their estimates (a decrease of 25% mOTUs is found when 6% was considered). Still, an overwhelming sampling effort but a more realistic estimate.
- I think the phylogenomic tree did not receive the required attention (for example, the FcLM analysis is barely mentioned).
- It is not clear why should be important to mention the "person-months of focused field research" across the manuscript. Each study group has a unique sampling technique (also not found in the manuscript), preferred localities or traits, which make comparisons impossible. The authors' effort is remarkable, but it is not an important result/finding to be highlighted all over the manuscript.
Many thanks for all comments and suggestions that pointed to the weak parts of our argumentation. We modified the manuscript accordingly and added some references that can be used for the justification of some claims.
We addressed the question of thresholds for species number estimations. Now, two thresholds are considered in the manuscript as relevant for discussion: 2% and 5%. We added further information on our previous studies dealing with integrative species delimitation in Metriorrhynchini. Some of them were not referred in the earlier version (to avoid self-citations) and we also expanded information on the evidence given in the study which we have already referenced (Bocek et al. 2019). The earlier comparison of nextRAd, mtDNA and moprhology-based delimitation of species in Eniclases (the trichaline clade in the present study) showed that many well defined species (nextRAD and morphology) have highly similar mtDNA and they split only recently, eventually some introgresion or incomplete lineage sorting affect mtDNA signal. If we apply 5% threshold for this group, we would delimit as a single species two entities which differ in the body size, coloration and the relative size of male eyes (diurnal and nocturnal activity in putative sister species). In such a way, we would decrease the number of species in our analyzed sample of Eniclases by 40% in clear contrast with the number based on morphology and nextRADs. We found similar rapid morphological diversification also in other metriorrhynchines (Jiruskova et al., 2019,; Kalousova & Bocak, 2017) and other not referenced taxonomic studies that have shown that closely related species have well diversified male genitalia and often belong to different mimetic rings). To limit our discussion, we do not reference our earlier nextRAD study showing the speciation in other subfamily of net-winged beetles within a single mountain range (Bray & Bocak 2016). Also this study supports morphological differentiation in species with highly similar mtDNA. Now, we noted in the manuscript that before taxonomic revisions are produced, our claim is provisional and therefore we modified the text as proposed and present the lower numbers of species as a realistic possibility.
Phylogenetic relationships: We added additional information on the congruence with earlier studies to Results and Discussion, but we still do not describe details. The main reason is that morphology must be studied to delimit and formally name new taxa and that the morphology is out of scope of this work (except some information provided in Supplementary Text – description of delimited generic groups and subtribes). The FcLM analysis addressed only the relative position of the leptotrichaline and procautirine clade. Both clades are monophyletic, morphologically distinct and no conclusion is based on their relative position. We noted that without further data we are unable to robustly solve their positions. Provisionally, we prefer the deeper postion of the leptotrichalines (61%, a not very convincing phylogenenomic signal).
Quantification of sampling effort: As proposed, we excluded the consideration of person months as a measure of relative collecting effort in various regions and add justification for field research methods.
Reviewer #2:
Conservation efforts must be evidence-based, so rapid and economically feasible methods should be used to quantify diversity and distribution patterns. The principal objective of this study is to demonstrate how biodiversity information for a hyperdiverse tropical group can be rapidly expanded via targeted field research and large-scale sequencing. The authors have attempted to overcome current impediments to the gathering of biodiversity data by using integrative phylogenomic and three mtDNA fragment analyses. As a model, they sequenced the Metriorrhynchini beetle fauna, sampled from ~700 localities in three continents. The species-rich dataset included ~6,500 terminals, >2,300 putative species, more than a half of them unknown to science. It is an amazing finding. Their information and phylogenetic hypotheses can be a resource for higher-level phylogenetics, population genetics, phylogeographic studies, and biodiversity estimation. At the same time, they want to show how limited the taxonomical knowledge is and how this lack is hindering biodiversity research and management.
Thanks for your comments on our study. We agree with your specific recommendations and modify the manuscript accordingly.
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Evaluation Summary:
This manuscript provides some clear ideas on the use of next-generation sequencing data to rapidly increase biodiversity inventories and set the basis for future research. The principal objective of this study is to demonstrate how biodiversity information for a hyperdiverse tropical group can be rapidly expanded via targeted field research and large-scale sequencing. The authors use a comprehensive sampling for a tribe of beetles with complicated morphological characters, highlight the existence of multiple undescribed taxa. The database of sequences could set a benchmark for the spatiotemporal evaluation of biodiversity, would support evidence-based conservation planning, and would provide a robust framework for systematic, biogeographic, and evolutionary studies.
(This preprint has been reviewed by eLife. We …
Evaluation Summary:
This manuscript provides some clear ideas on the use of next-generation sequencing data to rapidly increase biodiversity inventories and set the basis for future research. The principal objective of this study is to demonstrate how biodiversity information for a hyperdiverse tropical group can be rapidly expanded via targeted field research and large-scale sequencing. The authors use a comprehensive sampling for a tribe of beetles with complicated morphological characters, highlight the existence of multiple undescribed taxa. The database of sequences could set a benchmark for the spatiotemporal evaluation of biodiversity, would support evidence-based conservation planning, and would provide a robust framework for systematic, biogeographic, and evolutionary studies.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Reviewer #1 (Public Review):
In this manuscript, the authors make use of next-generation sequencing to provide a preliminary inventory of tribe Metriorrhynchini, a hyperdiverse group of beetles with intricate systematics mainly due to likely morphological convergence of their Millerian rings. The authors provide an admirable sampling within Africa, Asia and Oceania, with about 700 successfully sampled localities and thousands of specimens.
The main result of the manuscript is the curated database of Metriorrhynchini that will be useful in future research. In addition, different statistical methods are used to provide an idea of the undescribed species within the tribe, the astonishing species richness in New Guinea or the use of phylogenomic data to explore major phylogenetic relationships. However, some of the author's claims should be …
Reviewer #1 (Public Review):
In this manuscript, the authors make use of next-generation sequencing to provide a preliminary inventory of tribe Metriorrhynchini, a hyperdiverse group of beetles with intricate systematics mainly due to likely morphological convergence of their Millerian rings. The authors provide an admirable sampling within Africa, Asia and Oceania, with about 700 successfully sampled localities and thousands of specimens.
The main result of the manuscript is the curated database of Metriorrhynchini that will be useful in future research. In addition, different statistical methods are used to provide an idea of the undescribed species within the tribe, the astonishing species richness in New Guinea or the use of phylogenomic data to explore major phylogenetic relationships. However, some of the author's claims should be questioned:
- Surprisingly, the authors rely on a very low threshold to identify mOTUs (2% in the manuscript). The authors refer to Hebert et al. (2003) and Eberle et al. (2020) to justify the threshold, but still, they are likely overestimating the number of mOTUs and thus, considering putative species what it may be different populations. Figure S17 provide estimates of mOTUs with different thresholds (1 to 10%), which rapidly decrease their estimates (a decrease of 25% mOTUs is found when 6% was considered). Still, an overwhelming sampling effort but a more realistic estimate.
- I think the phylogenomic tree did not receive the required attention (for example, the FcLM analysis is barely mentioned).
- It is not clear why should be important to mention the "person-months of focused field research" across the manuscript. Each study group has a unique sampling technique (also not found in the manuscript), preferred localities or traits, which make comparisons impossible. The authors' effort is remarkable, but it is not an important result/finding to be highlighted all over the manuscript.
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Reviewer #2 (Public Review):
Conservation efforts must be evidence-based, so rapid and economically feasible methods should be used to quantify diversity and distribution patterns. The principal objective of this study is to demonstrate how biodiversity information for a hyperdiverse tropical group can be rapidly expanded via targeted field research and large-scale sequencing. The authors have attempted to overcome current impediments to the gathering of biodiversity data by using integrative phylogenomic and three mtDNA fragment analyses. As a model, they sequenced the Metriorrhynchini beetle fauna, sampled from ~700 localities in three continents. The species-rich dataset included ~6,500 terminals, >2,300 putative species, more than a half of them unknown to science. It is an amazing finding. Their information and phylogenetic …
Reviewer #2 (Public Review):
Conservation efforts must be evidence-based, so rapid and economically feasible methods should be used to quantify diversity and distribution patterns. The principal objective of this study is to demonstrate how biodiversity information for a hyperdiverse tropical group can be rapidly expanded via targeted field research and large-scale sequencing. The authors have attempted to overcome current impediments to the gathering of biodiversity data by using integrative phylogenomic and three mtDNA fragment analyses. As a model, they sequenced the Metriorrhynchini beetle fauna, sampled from ~700 localities in three continents. The species-rich dataset included ~6,500 terminals, >2,300 putative species, more than a half of them unknown to science. It is an amazing finding. Their information and phylogenetic hypotheses can be a resource for higher-level phylogenetics, population genetics, phylogeographic studies, and biodiversity estimation. At the same time, they want to show how limited the taxonomical knowledge is and how this lack is hindering biodiversity research and management.
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