Host separation syndrome and chemical dependency of ectosymbiotic decapods associated with echinoderms
(2023)
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- Symbiotic relationships, defined as close and long-lasting associations between at least two different species, are ubiquitous throughout the biosphere. One key factor that sustains symbioses across generations is the establishment of a host-specific chemical environment allowing, amongst others, the survival of the symbiont and its ability to select a suitable host. These chemical signals, true metabolites from the host, are also known as kairomones as they provide benefits for the symbiont. In echinoderms, the nature of the kairomones attracting symbionts is only known for associations involving sea cucumbers and sea urchins hosts. Moreover, when separated from their hosts, the environment (both chemical and nutritional) of the symbionts becomes unsuitable leading to a "host separation syndrome". This syndrome, only described in a sea urchin-shrimps association, is characterized by an alteration of the behavior and the state of health, potentially leading to the death of symbionts. The general aim of this thesis is to contribute to the knowledge of these kairomones playing a crucial role in symbiotic associations, notably those associating decapods with echinoderms which are frequent symbioses in the marine environment. First, the chemical characterization of the kairomonal chemical signature allowing host recognition was investigated in crinoid and asteroid hosts. Then, the host separation on various symbiotic decapods was monitored to characterize the syndrome in several species and to understand its impact at the behavioral, anatomical and physiological levels. The introduction of this thesis begins with a review of the diversity of macro-ectosymbiotic decapods associated with echinoderms. This includes an exhaustive list of 220 decapod species associated with all five classes of echinoderms, and an analysis of all these associations, described since 1849. The review also investigated association characteristics, such as the benefits for symbionts and their dependency on hosts, as well as co-evolution involving morphological, physiological, and behavioral adaptations. The introduction is followed by four chapters that provide new insights on the host separation syndrome and the host chemical dependency of decapod symbionts. Chapter I characterizes the chemical environment produced by crinoids and explores host recognition behavior in the symbiotic pistol shrimp, Synalpheus stimpsonii. The chemical attractiveness of two crinoid hosts and one non-host species, as well as commercial anthraquinones, were tested in an olfactometer. Mass spectrometry revealed, from the chemical extraction of the crinoid Phanogenia distincta, the presence of three different anthraquinones (rhodoptilometrin, comantherin, and a new crinoid anthraquinone) that trigger host recognition. Chapter II investigates host recognition in the adult and larvae of the shrimp Zenopontonia soror, an obligate symbiont of sea stars. Semiochemicals influencing host selection were revealed using chemical extractions, behavioral experiments in olfactometers, and mass spectrometry analyses. Our results demonstrate that asterosaponins are species-specific and play a role in host recognition, including symbiont larval recruitment. While adult shrimps were attracted only by their original host species Culcita novaeguineae, larvae were attracted by different asteroid species. This study provides, for the first time, the chemical identification of an olfactory cue used by larvae of symbiotic organisms to locate their hosts for recruitment. Chapter III explored the host separation syndrome using a transcriptomic approach. Paired-end Illumina HiSeq technology has been used to analyze transcriptomes from Arete indicus and Tuleariocaris holthuisi confronted with three different conditions used previously to investigate host separation syndrome. The three conditions analyzed were: individuals associated with their host, individuals separated from their host and individuals separated from their host but conditioned by naphthoquinones that is a kairomone involved in the host recognition by these symbionts. A total of 217,832 assembled unigenes were obtained, with an N50 of 2,061 bp. Our results show a proportion of 16.5% of differentially expressed genes in isolated T. holthuisi shrimp compared to the control treatment and a proportion of 8.5% of DEGs in isolated T. holthuisi shrimps in presence of spinochromes compared to the control. For A. indicus, there were fewer variations in DEG proportions among the same comparisons. Yet, analyses highlight a complex transcriptomic effect on both symbiotic species, with notably a differential expression of heat shock protein in isolated T. holthuisi. Chapter IV focuses on the mimetic pigmentation of four symbiotic models: Z. soror – C. novaeguineae, S. stimpsonii – P. distincta, T. holthuisi – E. mathaei and A. indicus – E. mathaei. The results suggested a strong host dependency of all four symbionts, but only three of them exhibited a host chemical dependency. The host isolation impacted the pigmentation of the symbionts, with a nuanced and dynamic pigmentation variation depending on the species. The chemical extraction highlights similar carotenoid pigments in Z. soror and C. novaeguineae. At the opposite, the crinoid P. distincta did not possess the carotenoids found in its associated shrimp. Histological sections show the presence of chromatophores in all the species and when shrimps discolored, their chromatophores agglomerated. The final discussion aims to incorporate the results obtained in the different thesis chapters to provide a broader understanding and potential future research objectives that may be carried out to better understand marine symbiotic associations and their integration in an ecosystem-level. It sheds light on the symbiont response to specific chemicals produced by the host and to the host separation. This research will contribute significantly to future studies on co-evolution, host recognition, and chemical ecology within symbiotic systems.
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Lourtie, A. (2023). Host separation syndrome and chemical dependency of ectosymbiotic decapods associated with echinoderms. https://hdl.handle.net/2078.5/269929