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Authors: Hartke, Juliane
Title: Cryptic species divergence and the evolution of cuticular hydrocarbon profiles in parabiotic ants
Online publication date: 10-Mar-2023
Year of first publication: 2023
Language: english
Abstract: The success of social insects is largely entwined with their elaborate communication system. Long-chained hydrocarbon molecules on the surface of insects make up specific profiles that function in species and nest-mate recognition, task allocation and mate-choice. Cuticular hydrocarbons (CHCs) thus facilitate the functioning of the sophisticated lifestyle of social insects, but aside from that also provide a barrier to pathogens and water loss. Due to this dual role in communication and ecological adaptation, CHCs are a strongly selected trait and are postulated to be drivers of rapid species divergence. This makes CHCs a particularly interesting trait to study, yet because of their dual role elucidating their genomic basis proved difficult in the past. Here, I examine the genomic basis of cuticular hydrocarbon diversity and evolution in mutualistic ants and investigate the interplay between CHC profiles and local environmental parameters. I focus on the two species Crematogaster levior and Camponotus femoratus that inhabit a shared nest, a so-called ant-garden, in large parts of the Amazonian rainforest. Both species were found to show striking diversity in their cuticular hydrocarbon profiles that were postulated to be a sign for cryptic species. This species complex thus provides an ideal model to study the evolution of CHC profiles either within highly diverse species or sister species. In the first chapter of this thesis, I elucidate species status of both Cr. levior and Ca. femoratus and show that both species split into morphologically nearly indistinguishable cryptic sister species (Cr. levior A and B, and Ca. femoratus PAT and PS) with exceptionally distinct CHC profiles. For this, morphometric measurements, DNA barcoding and the analysis of CHC profiles were combined in an integrative approach and provide three lines of conclusive evidence for the existence of cryptic species. I furthermore examine the distribution of the single species across the sampling range in French Guiana and find that in both Crematogaster species, the distribution is sympatric and independent of climate, in contrast to the two Camponotus species that show discrete distributions dependent on temperature and precipitation. The second chapter focuses on a detailed characterization of the cuticular hydrocarbon profiles of all four species. We conclude that mutualisms might lead to longer chain lengths that are, due to their physical properties, not suited for communication and thus may represent a case of chemical insignificance to facilitate acceptance of the mutualistic partner. We furthermore compared CHC profiles between the species and found signals of the parabiotic partner within CHC profiles, possibly pointing to a form of chemical mimicry as an adaptation to the mutualistic lifestyle. We also found that climate had a significant influence on the CHC profiles of all species, underlining the importance of cuticular hydrocarbons in ecological adaptation. As a basis for genome-wide analyses and to enable the identification of genes implicated in synthesis and detection of cuticular hydrocarbons, I sequenced the genome of one of the parabiotic ants, Cr. levior A. As described in chapter three, I used a combination of three different sequencing techniques and short and long reads to gain a highly accurate and contiguous depiction of the genome. Annotation of the genome showed an unusually high number of desaturases and a high number of elongases in this species, that might underly the increased chain lengths and specific adaptation to the mutualistic lifestyle. Comparisons to 40 other Hymenopteran species revealed a general expansion of both of those gene families within the order of Formicidae and an especially massive expansion of desaturases within Cr. levior A, which may be reflective of their complex mutualistic lifestyle. The genome was used as a basis for genome-wide population genomic analyses in both Cr. levior species, as detailed in chapter four. By correlating population-specific allele frequencies to climate and chemical parameters, I identified candidate genes implicated in climate adaptation as well as the synthesis and detection of CHCs. Noticeably, different odorant receptors are implicated in climate adaptation, a correlation that has not been shown before. Additionally, odorant receptors were also correlated to population-specific CHC profiles, underlining their suggested importance in the elaborate communication system of social insects. Signatures of selection showed no overlap between the cryptic species despite shared selection pressures, confirming the patterns of haphazard evolutionary mechanisms found in other studies. In conclusion, this thesis provides a closer look at a complex system of mutualistic ants. I present proof that both mutualistic partners encompass two cryptic species. I point to possible mechanisms that drove speciation in both cases, which most likely differed between the genera. Detailed analyses of signatures of selection among cryptic Cr. levior species show little overlap and solidify claims that evolution acts largely unpredictably. I identify candidate genes underlying communication and climate adaptation and thus provide a solid basis for future studies of the evolutionary trajectories of cuticular hydrocarbons and the intricate interplay of CHC synthesis, detection and their role in climate adaptation.
DDC: 570 Biowissenschaften
570 Life sciences
Institution: Johannes Gutenberg-Universität Mainz
Department: FB 10 Biologie
Place: Mainz
URN: urn:nbn:de:hebis:77-openscience-36a175f6-c096-41b7-9943-34db61daf73c9
Version: Original work
Publication type: Dissertation
License: In Copyright
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Extent: 184 Seiten ; Illustrationen, Diagramme
Appears in collections:JGU-Publikationen

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