The evolution and genomic basis of beetle diversity McKenna, Duane D.; Shin, Seunggwan; Ahrens, Dirk ...
Proceedings of the National Academy of Sciences - PNAS,
12/2019, Letnik:
116, Številka:
49
Journal Article
Recenzirano
Odprti dostop
The order Coleoptera (beetles) is arguably the most speciose group of animals, but the evolutionary history of beetles, including the impacts of plant feeding (herbivory) on beetle diversification, ...remain poorly understood. We inferred the phylogeny of beetles using 4,818 genes for 146 species, estimated timing and rates of beetle diversification using 89 genes for 521 species representing all major lineages and traced the evolution of beetle genes enabling symbiont-independent digestion of lignocellulose using 154 genomes or transcriptomes. Phylogenomic analyses of these uniquely comprehensive datasets resolved previously controversial beetle relationships, dated the origin of Coleoptera to the Carboniferous, and supported the codiversification of beetles and angiosperms. Moreover, plant cell wall-degrading enzymes (PCWDEs) obtained from bacteria and fungi via horizontal gene transfers may have been key to the Mesozoic diversification of herbivorous beetles—remarkably, both major independent origins of specialized herbivory in beetles coincide with the first appearances of an arsenal of PCWDEs encoded in their genomes. Furthermore, corresponding (Jurassic) diversification rate increases suggest that these novel genes triggered adaptive radiations that resulted in nearly half of all living beetle species. We propose that PCWDEs enabled efficient digestion of plant tissues, including lignocellulose in cell walls, facilitating the evolution of uniquely specialized plant-feeding habits, such as leaf mining and stem and wood boring. Beetle diversity thus appears to have resulted from multiple factors, including low extinction rates over a long evolutionary history, codiversification with angiosperms, and adaptive radiations of specialized herbivorous beetles following convergent horizontal transfers of microbial genes encoding PCWDEs.
The ages of cladogenetic events in Coleoptera are frequently estimated with mitochondrial protein-coding genes (MPCGs) and the “standard” mitochondrial nucleotide substitution rate for arthropods. ...This rate has been used for different mitochondrial gene combinations and time scales despite it was estimated on short mitochondrial sequences from few comparisons of close related species. These shortcomings may cause greater impact at deep phylogenetic levels as errors in rates and ages increase with branch lengths. We use the full set of MPCGs of 15 species of beetles (two of them newly sequenced here) to estimate the nucleotide evolutionary rates in a reconstructed phylogeny among suborders, paying special attention to the effect of data partitioning and model choices on these estimations. The optimal strategy for nucleotide data, as measured with Bayes factors, was partitioning by codon position. This retrieved Adephaga as a sister group to Myxophaga with strong support (expected-likelihood weights test 0.94–1) and both sisters to Polyphaga, in contradiction with the most currently accepted views. The hypothesis of Archostemata being sister to the remaining Coleoptera, which is in agreement with morphology, was increasingly supported when third codon sites were recoded or completely removed, sequences were analyzed as AA, and heterogeneous models were implemented but the support levels remained low. Nucleotide substitution rates were strongly affected by the choice of data partitioning (codon position
versus individual genes), with up to sixfold levels of variation, whereas differences in the molecular clock algorithm produced changes of only about 20%. The global mitochondrial protein coding rate using codon partitioning and an estimated age of 250 million years (MY) for the origin of the Coleoptera was 1.34% per branch per MY, which closely matches the ‘standard’ clock of 1.15% per MY. The estimation of the rates on alternative topologies gave similar results. Using local molecular clocks, the evolutionary rate in the Polyphaga and Archostemata was estimated to be nearly twice as fast as in the Adephaga and Myxophaga (1.03%
versus 0.53% per MY). Rates across individual genes varied from 0.55% to 8.61% per MY. Our results suggest that
cox1 might not be an optimal gene for implementing molecular clocks in deep phylogenies for beetles because it shows relatively slow rates at first and second codon positions but very fast rates at third ones. In contrast,
nad5,
nad4 and
nad2 perform better, as they exhibit more homogeneous rates among codon positions.
Detailed information about the known species groups of
Broun, 1886 from New Guinea is presented, including species numbers, distribution, and references of species-group diagnoses, keys to the ...species, and species descriptions. An identification key to all species groups is provided. Phylogeny and morphological character evolution are discussed.
The demand for scientific biodiversity data is increasing, but taxonomic expertise is often limited or not available. DNA sequencing is a potential remedy to overcome this taxonomic impediment. ...Mitochondrial DNA is most commonly used, e.g., for species identification ("DNA barcoding"). Here, we present the first study in arthropods based on a near-complete species sampling of a family-level taxon from the entire Australian region. We aimed to assess how reliably mtDNA data can capture species diversity when many sister species pairs are included. Then, we contrasted phylogenetic subsampling with the hitherto more commonly applied geographical subsampling, where sister species are not necessarily captured.
We sequenced 800 bp cox1 for 1,439 individuals including 260 Australian species (78% species coverage). We used clustering with thresholds of 1 to 10% and general mixed Yule Coalescent (GMYC) analysis for the estimation of species richness. The performance metrics used were taxonomic accuracy and agreement between the morphological and molecular species richness estimation. Clustering (at the 3% level) and GMYC reliably estimated species diversity for single or multiple geographic regions, with an error for larger clades of lower than 10%, thus outperforming parataxonomy. However, the rates of error were higher for some individual genera, with values of up to 45% when very recent species formed nonmonophyletic clusters. Taxonomic accuracy was always lower, with error rates above 20% and a larger variation at the genus level (0 to 70%). Sørensen similarity indices calculated for morphospecies, 3% clusters and GMYC entities for different pairs of localities was consistent among methods and showed expected decrease over distance.
Cox1 sequence data are a powerful tool for large-scale species richness estimation, with a great potential for use in ecology and β-diversity studies and for setting conservation priorities. However, error rates can be high in individual lineages.
The German Barcoding initiatives BFB and GBOL have generated a reference library of more than 16,000 metazoan species, which is now ready for applications concerning next generation molecular ...biodiversity assessments. To streamline the barcoding process, we have developed a meta-barcoding pipeline: We pre-sorted a single malaise trap sample (obtained during one week in August 2014, southern Germany) into 12 arthropod orders and extracted DNA from pooled individuals of each order separately, in order to facilitate DNA extraction and avoid time consuming single specimen selection. Aliquots of each ordinal-level DNA extract were combined to roughly simulate a DNA extract from a non-sorted malaise sample. Each DNA extract was amplified using four primer sets targeting the CO1-5' fragment. The resulting PCR products (150-400bp) were sequenced separately on an Illumina Mi-SEQ platform, resulting in 1.5 million sequences and 5,500 clusters (coverage ≥10; CD-HIT-EST, 98%). Using a total of 120,000 DNA barcodes of identified, Central European Hymenoptera, Coleoptera, Diptera, and Lepidoptera downloaded from BOLD we established a reference sequence database for a local CUSTOM BLAST. This allowed us to identify 529 Barcode Index Numbers (BINs) from our sequence clusters derived from pooled Malaise trap samples. We introduce a scoring matrix based on the sequence match percentages of each amplicon in order to gain plausibility for each detected BIN, leading to 390 high score BINs in the sorted samples; whereas 268 of these high score BINs (69%) could be identified in the combined sample. The results indicate that a time consuming presorting process will yield approximately 30% more high score BINs compared to the non-sorted sample in our case. These promising results indicate that a fast, efficient and reliable analysis of next generation data from malaise trap samples can be achieved using this pipeline.
The evolution of the coleopteran suborder Adephaga is discussed based on a robust phylogenetic background. Analyses of morphological characters yield results nearly identical to recent molecular ...phylogenies, with the highly specialized Gyrinidae placed as sister to the remaining families, which form two large, reciprocally monophyletic subunits, the aquatic Haliplidae + Dytiscoidea (Meruidae, Noteridae, Aspidytidae, Amphizoidae, Hygrobiidae, Dytiscidae) on one hand, and the terrestrial Geadephaga (Trachypachidae + Carabidae) on the other. The ancestral habitat of Adephaga, either terrestrial or aquatic, remains ambiguous. The former option would imply two or three independent invasions of aquatic habitats, with very different structural adaptations in larvae of Gyrinidae, Haliplidae and Dytiscoidea.
This study presents the largest set of morphological characters of adults and immature stages ever compiled for the coleopteran suborder Adephaga.
Analyses of the morphological characters yield results nearly identical to recent analyses of molecular data, suggesting that a stable phylogeny has been achieved.
The character transformation on the phenotypic level is reconstructed using a formal approach for the first time, based on the robust phylogenetic pattern and mesquite.
Aim: The respective contribution of vicariance and/or dispersal events to the evolution of clades dwelling in the archipelagic parts of the Oriental and Australian regions remains equivocal. Using a ...complete, species-level phylogeny of Polyura butterflies that are widespread in the oriental Palaeotropics, we aim to test predictions related to vicariance driven by past abiotic factors in the Indo-Australian archipelago (IAA) (Miocene tectonics and Pleistocene climatic shifts) versus repeated trans-archipelagic dispersal events. Location: The Oriental and Australian regions with a focus on the IAA. Methods: Bayesian species tree phylogenetic analyses were conducted using a matrix comprising two mitochondrial and two nuclear gene fragments. Bayesian relaxed clocks were used to produce a chronogram, which was used in ancestral area estimations to infer the spatio-temporal evolution of the genus at different geographical scales. Diversification dynamics were investigated using the package TreePar in R. Results: Polyura originated during the mid-Miocene (c. 13 million years ago).Ancestral area estimations inferred an origin in Indomalaya. Wallacea was colonized out-of-Indomalaya in the P. pyrrhus group, while the P. athamas and P.eudamippus groups diversified in Indomalaya and the east Palaearctic. We inferred three long-distance dispersal (LDD) events. The first one implies outof-Sunda colonization of the Solomon Islands, which have three extant, endemic species. The second implies a colonization of Vanuatu out-of-Sunda that later served as a stepping stone for the colonization of other Pacific islands (Fiji and New Caledonia). A third permitted the reverse colonization of Wallacea from the Pacific islands. These LDD events were supported by our diversification analyses that suggested no diversification rate shift throughout the evolution of the genus. Main conclusions: Our results suggest unusual colonization routes with Pacific islands as a hub for late Miocene reverse colonizations back into the centre of the Indo-Australian archipelago.
The Austrelatus papuensis group is the second species group of the New Guinean representatives of the recently described genus Austrelatus Shaverdo et al., 2023. The group is mainly defined by ...distinct scale- and/or spinula-like surface structures of the dorsal sclerite of the median lobe. The species group already contains four described species and 42 new species and one subspecies treated here: Austrelatus aiyurensis sp. nov. , A. asteios sp. nov. , A. bewaniensis sp. nov. , A. bosaviensis sp. nov. , A. bundunensis sp. nov. , A. centralensis sp. nov. , A. craterensis sp. nov. , A. decoris sp. nov. , A. dekai sp. nov. , A. epicharis sp. nov. , A. flavocapitatus sp. nov. , A. fuscus sp. nov. , A. herzogensis sp. nov. , A. inconstans sp. nov. , A. iriatoi sp. nov. , A. kalibumi sp. nov. , A. kebarensis sp. nov. , A. kokodensis sp. nov. , A. leptos sp. nov. , A. loloki sp. nov. , A. lopintolensis sp. nov. , A. madangensis sp. nov. , A. maindai sp. nov. , A. mamberamo sp. nov. , A. mianminensis sp. nov. , A. miltokarenos sp. nov. , A. noiadi sp. nov. , A. normanbyensis sp. nov. , A. ohu sp. nov. , A. posmani sp. nov. , A. procerus sp. nov. , A. pseudogestroi sp. nov. , A. pseudomianminensis sp. nov. , A. robustus sp. nov. , A. sararti sp. nov. , A. sumokedi sp. nov. , A. wanangensis sp. nov. , A. wasiorensis sp. nov. , A. wasurensis sp. nov. , A. weigeli sp. nov. , A. yamurensis sp. nov. , A. yeretuar sp. nov. , A. xanthocephalus nabirensis ssp. nov. A checklist and identification key to New Guinean species of the group are provided and important diagnostic characters are illustrated. Data on the species distributions and habiat preferences are given.
Beetles represent almost one-fourth of all described species, and knowledge about their relationships and evolution adds to our understanding of biodiversity. We performed a comprehensive ...phylogenetic analysis of Coleoptera inferred from three genes and nearly 1900 species, representing more than 80% of the world's recognized beetle families. We defined basal relationships in the Polyphaga supergroup, which contains over 300,000 species, and established five families as the earliest branching lineages. By dating the phylogeny, we found that the success of beetles is explained neither by exceptional net diversification rates nor by a predominant role of herbivory and the Cretaceous rise of angiosperms. Instead, the pre-Cretaceous origin of more than 100 present-day lineages suggests that beetle species richness is due to high survival of lineages and sustained diversification in a variety of niches.
PDF
