Showing papers by "Niklas Wahlberg published in 2021"

Toward a Stable Global Noctuidae (Lepidoptera) Taxonomy

Abstract: Noctuidae are one of the world's most diverse, ecologically successful, and economically important animal lineages with over 12,000 species in ∼1,150 genera. We inferred a phylogeny using eight protein-coding genes for the global fauna, greatly expanding upon previous attempts to stabilize Noctuidae higher classification by sampling 341 genera (nearly half represented by their type species) representing 70/76 widely recognized family-group taxa: 20/21 subfamilies, 32/35 tribes, and 18/20 subtribes. We evaluated 17 subfamily-level taxa in detail, discussing adult and larval morphology, life histories, and taxonomic implications of our results. We significantly alter concepts of Acontiinae, Condicinae, Eustrotiinae, Metoponiinae, and Stiriinae. Our results supported recognition of two new subfamilies: Cobubathinae Wagner & Keegan, 2021 subf. nov. and Cropiinae Keegan & Wagner, 2021 subf. nov. Other nomenclatural changes we made are as follows. We moved: 'Acontia' viridifera (Hampson, 1910), 'Azenia' virida Barnes and McDunnough, 1916, Aleptinoides, Austrazenia, Chalcoecia, Megalodes, and Trogotorna to Chamaecleini in Acontiinae; Apaustis to, and reinstated Emmelia as a valid genus in Acontiinae; Allophyes and Meganephria to Cuculliinae; 'Plagiomimicus' navia (Harvey, 1875), Airamia, Alvaradoia, Hypoperigea, Neotarache, and Mesotrosta to Condicinae; Axenus, Azenia, Metaponpneumata, Sexserrata, and Tristyla to Metoponiinae; 'Paramiana' canoa (Barnes, 1907) to Noctuinae; Aucha, Cobubatha, and Tripudia to Cobubathinae; Anycteola and Supralathosea to Oncocnemidinae; Cropia to Cropiinae; Desmoloma to Dyopsinae; Eviridemas and Gloanna to Bryophilinae; Fota and Stilbia to Stiriinae; and Copibryophila, Homolagoa, and Tyta to Noctuidae incertae sedis. We conclude with discussion of instances where current understanding of noctuid biogeography and life histories were changed by our results. (Less)

Conserved ancestral tropical niche but different continental histories explain the latitudinal diversity gradient in brush-footed butterflies

Abstract: The global increase in species richness toward the tropics across continents and taxonomic groups, referred to as the latitudinal diversity gradient, stimulated the formulation of many hypotheses to explain the underlying mechanisms of this pattern. We evaluate several of these hypotheses to explain spatial diversity patterns in a butterfly family, the Nymphalidae, by assessing the contributions of speciation, extinction, and dispersal, and also the extent to which these processes differ among regions at the same latitude. We generate a time-calibrated phylogeny containing 2,866 nymphalid species (~45% of extant diversity). Neither speciation nor extinction rate variations consistently explain the latitudinal diversity gradient among regions because temporal diversification dynamics differ greatly across longitude. The Neotropical diversity results from low extinction rates, not high speciation rates, and biotic interchanges with other regions are rare. Southeast Asia is also characterized by a low speciation rate but, unlike the Neotropics, is the main source of dispersal events through time. Our results suggest that global climate change throughout the Cenozoic, combined with tropical niche conservatism, played a major role in generating the modern latitudinal diversity gradient of nymphalid butterflies. A phylogeny of Nymphalidae butterflies unveils the origin of the latitudinal diversity gradient. This study showed that the modern pattern of species richness emerged from dynamics of dispersal and diversification that varied through time and across regions, and that global climate change throughout the Cenozoic probably played a major role in generating the biodiversity pattern.

Mesoamerica is a cradle and the Atlantic Forest is a museum of Neotropical butterfly diversity: insights from the evolution and biogeography of Brassolini (Lepidoptera: Nymphalidae)

Abstract: Regional species diversity is ultimately explained by speciation, extinction, and dispersal. Here we estimate dispersal and speciation rates of Neotropical butterflies to propose an explanation for their distribution and diversity of extant species. We focus on the tribe Brassolini (owl butterflies and allies): a Neotropical group that comprises 17 genera and 108 species, most of them endemic to rainforest biomes. We infer a robust species tree using the multispecies coalescent framework and a dataset including molecular and morphological characters. This formed the basis for three changes in Brassolini classification: 1) Naropina, SYN. NOV. is subsumed within Brassolina; 2) Aponarope, SYN. NOV. is subsumed within Narope; 3) Selenophanes orgetorix, COMB. NOV. is reassigned from Catoblepia to Selenophanes. By applying biogeographical stochastic mapping, we found contrasting species diversification and dispersal dynamics across rainforest biomes, which might be partly explained by the geological and environmental history of each bioregion. Our results reveal a mosaic of biome-specific evolutionary histories within the Neotropics, where butterfly species have diversified rapidly (cradles: Mesoamerica), have accumulated gradually (museums: Atlantic Forest), or have alternately diversified and accumulated (Amazonia). Our study contributes evidence from a major butterfly lineage that the Neotropics are a museum and cradle of species diversity.

Wolbachia affects mitochondrial population structure in two systems of closely related Palaearctic blue butterflies

Abstract: The bacterium Wolbachia infects many insect species and spreads by diverse vertical and horizontal means. As co-inherited organisms, these bacteria often cause problems in mitochondrial phylogeny inference. The phylogenetic relationships of many closely related Palaearctic blue butterflies (Lepidoptera: Lycaenidae: Polyommatinae) are ambiguous. We considered the patterns of Wolbachia infection and mitochondrial diversity in two systems: Aricia agestis/Aricia artaxerxes and the Pseudophilotes baton species complex. We sampled butterflies across their distribution ranges and sequenced one butterfly mitochondrial gene and two Wolbachia genes. Both butterfly systems had uninfected and infected populations, and harboured several Wolbachia strains. Wolbachia was highly prevalent in A. artaxerxes and the host’s mitochondrial structure was shallow, in contrast to A. agestis. Similar bacterial alleles infected both Aricia species from nearby sites, pointing to a possible horizontal transfer. Mitochondrial history of the P. baton species complex mirrored its Wolbachia infection and not the taxonomical division. Pseudophilotes baton and P. vicrama formed a hybrid zone in Europe. Wolbachia could obscure mitochondrial history, but knowledge on the infection helps us to understand the observed patterns. Testing for Wolbachia should be routine in mitochondrial DNA studies.

Museomics: Phylogenomics of the Moth Family Epicopeiidae (Lepidoptera) Using Target Enrichment

Abstract: Billions of specimens can be found in natural history museum collections around the world, holding potential molecular secrets to be unveiled. Among them are intriguing specimens of rare families of moths that, while represented in morphology-based works, are only beginning to be included in genomic studies: Pseudobistonidae, Sematuridae, and Epicopeiidae. These three families are part of the superfamily Geometroidea, which has recently been defined based on molecular data. Here we chose to focus on these three moth families to explore the suitability of a genome reduction method, target enrichment (TE), on museum specimens. Through this method, we investigated the phylogenetic relationships of these families of Lepidoptera, in particular the family Epicopeiidae. We successfully sequenced 25 samples, collected between 1892 and 2001. We use 378 nuclear genes to reconstruct a phylogenetic hypothesis from the maximum likelihood analysis of a total of 36 different species, including 19 available transcriptomes. The hypothesis that Sematuridae is the sister group of Epicopeiidae + Pseudobistonidae had strong support. This study thus adds to the growing body of work, demonstrating that museum specimens can successfully contribute to molecular phylogenetic studies.

Museomics of a rare taxon: placing Whalleyanidae in the Lepidoptera Tree of Life

Abstract: Museomics is a valuable approach that utilizes the diverse biobanks that are natural history museums. The ability to sequence genomes from old specimens has expanded not only the variety of interesting taxa available to study but also the scope of questions that can be investigated in order to further knowledge about biodiversity. Here, we present whole genome sequencing results from the enigmatic genus Whalleyana (comprising two species – occurring in drier biomes of Madagascar – previously placed in a monotypic superfamily, Whalleyanoidea), as well as from certain species of the families Callidulidae and Hyblaeidae (Calliduloidea and Hyblaeoidea, respectively). Library preparation was carried out on four museum specimens and one existing DNA extract and sequenced with Illumina short reads. De novo assembly resulted in highly fragmented genomes with the N50 ranging from 317 to 2078 bp. Mining of a manually curated gene set of 331 genes from these draft genomes had an overall gene recovery rate of 64–90%. Phylogenetic analysis places Whalleyana as sister to Callidulidae and Hyblaea as sister to Pyraloidea. Since the former sister-group relationship turns out to be also supported by ten morphological synapomorphies, we propose to formally assign the Whalleyanidae to the superfamily Calliduloidea. These results highlight the usefulness of not only museum specimens but also existing DNA extracts, for whole genome sequencing and gene mining for phylogenomic studies.

Miocene Climate and Habitat Change Drove Diversification in Bicyclus, Africa's Largest Radiation of Satyrine Butterflies.

Abstract: Compared to other regions, the drivers of diversification in Africa are poorly understood. We studied a radiation of insects with over 100 species occurring in a wide range of habitats across the Afrotropics to investigate the fundamental evolutionary processes and geological events that generate and maintain patterns of species richness on the continent. By investigating the evolutionary history of Bicyclus butterflies within a phylogenetic framework, we inferred the group's origin at the Oligo-Miocene boundary from ancestors in the Congolian rainforests of central Africa. Abrupt climatic fluctuations during the Miocene (ca. 19-17 Ma) likely fragmented ancestral populations, resulting in at least eight early-divergent lineages. Only one of these lineages appears to have diversified during the drastic climate and biome changes of the early Miocene, radiating into the largest group of extant species. The other seven lineages diversified in forest ecosystems during the late Miocene and Pleistocene when climatic conditions were more favourable-warmer and wetter. Our results suggest changing Neogene climate, uplift of eastern African orogens, and biotic interactions might have had different effects on the various subclades of Bicyclus, producing one of the most spectacular butterfly radiations in Africa.

Airborne environmental DNA metabarcoding for the monitoring of terrestrial insects - a proof of concept

Abstract: Biodiversity is in decline due to human land use, exploitation, and climate change. To be able to counteract this alarming trend it is paramount to closely monitor biodiversity at global scales. Because this is practically impossible with traditional methods, the last decade has seen a strong push for solutions. In aquatic ecosystems the monitoring of species from environmental DNA (eDNA) has emerged as one of the most powerful tools at our disposal but in terrestrial ecosystems the power of eDNA for monitoring has so far been hampered by the local scale of the samples. In this study we report the first attempt to detect insects from airborne eDNA. We compare our results to two traditional insect monitoring projects (1) using light trapping for moth monitoring and (2) transect counts for the monitoring of butterflies and wild bees. While we failed to detect many of the same species monitored with the traditional methods, airborne eDNA metabarcoding revealed DNA from from six classes of Arthropods, and twelve order of Insects - including representatives from all of the four largest orders: Diptera (flies), Lepidoptera (butterflies and moths), Coleoptera (beetles) and Hymenoptera (bees, wasps and ants). We also recovered DNA from nine species of vertebrates, including frogs, birds and mammals as well as from 12 other phyla. We suggest that airborne eDNA has the potential to become a powerful tool for terrestrial biodiversity monitoring, with many impactful applications including the monitoring of pests, invasive or endangered species or disease vectors.

The (non) accuracy of mitochondrial genomes for family level phylogenetics: the case of erebid moths (Lepidoptera; Erebidae)

Abstract: The use of molecular data to study evolutionary history of different organisms, revolutionized the field of systematics. Now with the appearance of high throughput sequencing (HTS) technologies more and more genetic sequence data is available. One of the important sources of genetic data for phylogenetic analyses has been mitochondrial DNA. The limitations of mitochondrial DNA for the study of phylogenetic relationships have been thoroughly explored in the age of single locus phylogenies. Now with the appearance of genomic scale data, more and more mitochondrial genomes are available. Here we assemble 47 mitochondrial genomes using whole genome Illumina short reads of representatives of the family Erebidae (Lepidoptera), in order to evaluate the accuracy of mitochondrial genome application in resolving deep phylogenetic relationships. We find that mitogenomes are inadequate for resolving subfamily level relationships in Erebidae, but given good taxon sampling, we see its potential in resolving lower level phylogenetic relationships.

A Database and checklist of geometrid moths (Lepidoptera) from Colombia

Abstract: Background Molecular DNA sequence data allow unprecedented advances in biodiversity assessments, monitoring schemes and taxonomic works, particularly in poorly-explored areas. They allow, for instance, the sorting of material rapidly into operational taxonomic units (such as BINs - Barcode Index Numbers), sequences can be subject to diverse analyses and, with linked metadata and physical vouchers, they can be examined further by experts. However, a prerequisite for their exploitation is the construction of reference libraries of DNA sequences that represent the existing biodiversity. To achieve these goals for Geometridae (Lepidoptera) moths in Colombia, expeditions were carried out to 26 localities in the northern part of the country in 2015-2019. The aim was to collect specimens and sequence their DNA barcodes and to record a fraction of the species richness and occurrences in one of the most biodiversity-rich countries. These data are the beginning of an identification guide to Colombian geometrid moths, whose identities are currently often provisional only, being morpho species or operational taxonomic units (OTUs). Prior to the current dataset, 99 Geometridae sequences forming 44 BINs from Colombia were publicly available on the Barcode of Life Data System (BOLD), covering 20 species only. New information We enrich the Colombian Geometridae database significantly by including DNA barcodes, two nuclear markers, photos of vouchers and georeferenced occurrences of 281 specimens of geometrid moths from different localities. These specimens are classified into 80 genera. Analytical tools on BOLD clustered 157 of the mentioned sequences to existing BINs identified to species level, identified earlier by experts. Another 115 were assigned to BINs that were identified to genus or tribe level only. Eleven specimens did not match any existing BIN on BOLD and are, therefore, new additions to the database. It is likely that many BINs represent undescribed species. Nine short sequences (< 500bp) were not assigned to BINs, but identified to the lowest taxonomic category by expert taxonomists and with comparisons of type material photos. The released new genetic information will help to further progress the systematics of Geometridae. An illustrated catalogue of all new records allows validation of our identifications; it is also the first document of this kind for Colombian Geometridae. All specimens are deposited at the Museo de Zoologia of Universidad de Sucre (MZUS), North Colombia. DNA BINs are reported in this study through dx.doi.org/10.5883/DS-GEOCO, the species occurrences are available on SIB Colombia https://sibcolombia.net/ and the Global Biodiversity Information Facility (GBIF) https://www.gbif.org/ through https://doi.org/10.15472/ucfmkh.

A double-edged sword: Unrecognized cryptic diversity and taxonomic impediment in Eois (Lepidoptera, Geometridae)

Abstract: The genus Eois Hubner (Geometridae: Larentiinae) comprises 254 valid species. Being a hyperdiverse genus, Eois potentially includes many undescribed cryptic species and embodies a problematic taxonomic scenario. The actual diversity of Eois is greatly underestimated and the Neotropical fauna needs to be well known since it figures as one of the most threatened terrestrial ecosystem. In the present study, we compare three species delimitation methods to highlight the hidden diversity within a subset of Eois species: Automatic Barcode Gap Discovery, Bayesian Poisson Tree Processes and Multi-Rate Poisson Tree Processes. Our results point to an increase up to 176% in the currently valid species number. The hypothesis of cryptic diversity is corroborated by morphological characters within some species complexes. For complexes comprising species of Brazilian fauna, we provide a preliminary taxonomic assessment. Additionally, we found no congruence among the three delimitation methods for some species complexes, which indicates the importance of species and locality sampling as well as the previous alpha taxonomic knowledge in avoiding result bias. In this sense, we tried to standardize the identification provided for the Genbank sequences used in most relevant publications for Eois, in order to minimize biases and maximize the replicability of analyses in future studies. Moreover, we stress the importance of an integrative taxonomic approach for cryptic species discovery approach by employing both morphological attributes and life history to corroborate molecular analysis.

Insect taxonomy can be difficult: a noctuid moth (Agaristinae: Aletopus imperialis) and a geometrid moth (Sterrhinae: Cartaletis dargei) combined into a cryptic species complex in eastern Africa (Lepidoptera)

Abstract: The systematic position of a large and strikingly coloured reddish-black moth, Cartaletis dargei Herbulot, 2003 (Geometridae: Sterrhinae) from Tanzania, has remained questionable since its description. Here we present molecular and morphological evidence showing that Cartaletis dargei only superficially resembles true Cartaletis Warren, 1894 (the relative name currently considered a junior synonym of Aletis Hubner, 1820), which are unpalatable diurnal moths superficially resembling butterflies, and that it is misplaced in the family Geometridae. We transfer it to Noctuidae: Agaristinae, and combine it with the genus Aletopus Jordan, 1926, from Tanzania, as Aletopus dargei (Herbulot, 2003) (new combination). We revise the genus Aletopus to contain three species, but find that it is a cryptic species complex that needs to be revised with more extensive taxon sampling. Our results demonstrate the difficulties in interpreting and classifying biological diversity. We discuss the problems in species delimitation and the potential drivers of evolution in eastern Africa that led to phenotypic similarity in unrelated lepidopteran lineages.

Alone on an island: The reassessment of an enigmatic species of Handmaiden Moth (Lepidoptera, Erebidae) endemic to Mauritius

Abstract: Maculonaclia florida (de Joannis, 1906) has been one of the most mysterious moths of Mauritius, a small volcanic island located some 900 km east from Madagascar. Here, we reviewed its generic placement, phylogenetic relationships and the potential evolutionary scenarios leading to the current distribution of this unique Mauritian member of Syntomini. The species, known previously only from a few old museum specimens, is redescribed based on newly collected material including both sexes and eggs. The generic affiliation to the Palaearctic Dysauxes is confirmed based on morphological and molecular data. A hypothesis is presented on the colonization of Mauritius by the ancestor of D. florida from Madagascar through the now submerged stepping stone islands of the Mascarene ridge. Behavioural data and environment preferences of D. florida are assessed for the first time. The species prefers shrubby vegetation with a humid understory, and presence of endemic shrub Ixora parviflora seems to play a role in selecting the suitable microhabitat. Additionally, based on IUCN criteria, a CR threat category is proposed, highlighting the major risk factors affecting the species. The significant variation in wing venation of D. florida is noted and provisionally correlated with environmental stress, which is the consequence of human-caused habitat degradation. Finally, the study provides further evidence for the significant role of Madagascar in the diversification of continental biota, indicating a Malagasy origin of the African syntomine Pseudonaclia puella.

The unresolved phylogenomic tree of butterflies and moths (Lepidoptera): assessing the potential causes and consequences

Abstract: The field of molecular phylogenetics is being revolutionised with next-generation sequencing technologies making it possible to sequence large numbers of genomes for non-model organisms ushering us into the era of phylogenomics. The current challenge is no longer how to get enough data, but rather how to analyse the data and how to assess the support for the inferred phylogeny. We focus on one of the largest animal groups on the planet – butterflies and moths (order Lepidoptera). We clearly demonstrate that there are unresolved issues in the inferred phylogenetic relationships of the major lineages, despite several recent phylogenomic studies of the group. We assess the potential causes and consequences of the conflicting phylogenetic hypotheses. With a dataset consisting of 331 protein-coding genes and the alignment length over 290 000 base pairs, including 200 taxa representing 81% of lepidopteran superfamilies, we compare phylogenetic hypotheses inferred from amino acid and nucleotide alignments. The resulting two phylogenies are discordant, especially with respect to the placement of the superfamily Gelechioidea, which is likely due to compositional bias of both the nucleotide and amino acid sequences. With a series of analyses, we dissect our dataset and demonstrate that there is sufficient phylogenetic signal to resolve much of the lepidopteran tree of life. Overall, the results from the nucleotide alignment are more robust to the various perturbations of the data that we carried out. However, the lack of support for much of the backbone within Ditrysia makes the current butterfly and moth tree of life still unresolved. We conclude that taxon sampling remains an issue even in phylogenomic analyses, and recommend that poorly sampled highly diverse groups, such as Gelechioidea in Lepidoptera, should receive extra attention in the future.

Mesoamerica is a cradle and the Atlantic Forest is a museum of Neotropical butterfly diversity: Insights from the evolution and biogeography of Brassolini (Lepidoptera: Nymphalidae)

Abstract: Regional species diversity is ultimately explained by speciation, extinction, and dispersal. Here we estimate dispersal and speciation rates of Neotropical butterflies to propose an explanation for their distribution and diversity of extant species. We focus on the tribe Brassolini (owl butterflies and allies): a Neotropical group that comprises 17 genera and 108 species, most of them endemic to rainforest biomes. We infer a robust species tree using the multispecies coalescent framework and a dataset including molecular and morphological characters. This formed the basis for three changes in Brassolini classification: 1) Naropina, SYN. NOV. is subsumed within Brassolina; 2) Aponarope, SYN. NOV. is subsumed within Narope; 3) Selenophanes orgetorix, COMB. NOV. is reassigned from Catoblepia to Selenophanes. By applying biogeographical stochastic mapping, we found contrasting species diversification and dispersal dynamics across rainforest biomes, which might be partly explained by the geological and environmental history of each bioregion. Our results reveal a mosaic of biome-specific evolutionary histories within the Neotropics, where butterfly species have diversified rapidly (cradles: Mesoamerica), have accumulated gradually (museums: Atlantic Forest), or have alternately diversified and accumulated (Amazonia). Our study contributes evidence from a major butterfly lineage that the Neotropics are a museum and cradle of species diversity.