Dataset Information

No impact of a short-term climatic "El Nino" fluctuation on gut microbial diversity in populations of the Galapagos marine iguana (Amblyrhynchus cristatus).

ABSTRACT: Gut microorganisms are crucial for many biological functions playing a pivotal role in the host's well-being. We studied gut bacterial community structure of marine iguana populations across the Galápagos archipelago. Marine iguanas depend heavily on their specialized gut microbiome for the digestion of dietary algae, a resource whose growth was strongly reduced by severe "El Niño"-related climatic fluctuations in 2015/2016. As a consequence, marine iguana populations showed signs of starvation as expressed by a poor body condition. Body condition indices (BCI) varied between island populations indicating that food resources (i.e., algae) are affected differently across the archipelago during 'El Niño' events. Though this event impacted food availability for marine iguanas, we found that reductions in body condition due to "El Niño"-related starvation did not result in differences in bacterial gut community structure. Species richness of gut microorganisms was instead correlated with levels of neutral genetic diversity in the distinct host populations. Our data suggest that marine iguana populations with a higher level of gene diversity and allelic richness may harbor a more diverse gut microbiome than those populations with lower genetic diversity. Since low values of these diversity parameters usually correlate with small census and effective population sizes, we use our results to propose a novel hypothesis according to which small and genetically less diverse host populations might be characterized by less diverse microbiomes. Whether such genetically depauperate populations may experience additional threats from reduced dietary flexibility due to a limited intestinal microbiome is currently unclear and calls for further investigation.

SUBMITTER: Ibanez A

PROVIDER: S-EPMC7854437 | biostudies-literature | 2021 Feb

REPOSITORIES: biostudies-literature

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No impact of a short-term climatic "El Niño" fluctuation on gut microbial diversity in populations of the Galápagos marine iguana (Amblyrhynchus cristatus).

Ibáñez Alejandro A Bletz Molly C MC Quezada Galo G Geffers Robert R Jarek Michael M Vences Miguel M Steinfartz Sebastian S

Die Naturwissenschaften 20210202 1

Gut microorganisms are crucial for many biological functions playing a pivotal role in the host's well-being. We studied gut bacterial community structure of marine iguana populations across the Galápagos archipelago. Marine iguanas depend heavily on their specialized gut microbiome for the digestion of dietary algae, a resource whose growth was strongly reduced by severe "El Niño"-related climatic fluctuations in 2015/2016. As a consequence, marine iguana populations showed signs of starvation ...[more]

PMID: 33528676

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Project description:The El Niño-Southern Oscillation (ENSO) is a major source of climatic disturbance, impacting the dynamics of ecosystems worldwide. Recent models predict that human-generated rises in green-house gas levels will cause an increase in the strength and frequency of El Niño warming events in the next several decades, highlighting the need to understand the potential biological consequences of increased ENSO activity. Studies have focused on the ecological and demographic implications of El Niño in a range of organisms, but there have been few systematic attempts to measure the impact of these processes on genetic diversity in populations. Here, we evaluate whether the 1997-1998 El Niño altered the genetic composition of Galápagos marine iguana populations from eleven islands, some of which experienced mortality rates of up to 90% as a result of El Niño warming. Specifically, we measured the temporal variation in microsatellite allele frequencies and mitochondrial DNA diversity (mtDNA) in samples collected before (1991/1993) and after (2004) the El Niño event. Based on microsatellite data, only one island (Marchena) showed signatures of a genetic bottleneck, where the harmonic mean of the effective population size (N(e)) was estimated to be less than 50 individuals during the period between samplings. Substantial decreases in mtDNA variation between time points were observed in populations from just two islands (Marchena and Genovesa). Our results suggests that, for the majority of islands, a single, intense El Niño event did not reduce marine iguana populations to the point where substantial neutral genetic diversity was lost. In the case of Marchena, simultaneous changes to both nuclear and mitochondrial DNA variation may also be the result of a volcanic eruption on the island in 1991. Therefore, studies that seek to evaluate the genetic impact of El Niño must also consider the confounding or potentially synergistic effect of other environmental and biological forces shaping populations.

Project description:BackgroundUnderstanding the natural microbiome and resistome of wildlife from remote places is necessary to monitor the human footprint on the environment including antimicrobial use (AU). Marine iguanas are endemic species from the Galapagos Islands where they are highly affected by anthropogenic factors that can alter their microbiota as well as their abundance and diversity of antimicrobial-resistant genes (ARGs). Thus, this study aims to apply culture-independent approaches to characterize the marine iguana's gut metagenomic composition of samples collected from the uninhabited islands Rabida (n = 8) and Fernandina (Cabo Douglas, n = 30; Punta Espinoza, n = 30). Fresh feces from marine iguanas were analyzed through SmartChip RT-PCR, 16S rRNA, and metagenomic next-generation sequencing (mNGS) to identify their microbiome, microbial-metabolic pathways, resistome, mobilome, and virulome.ResultsThe marine iguana's gut microbiome composition was highly conserved despite differences in ecological niches, where 86% of taxa were shared in the three locations. However, site-specific differences were mainly identified in resistome, mobilome, virulorome, and metabolic pathway composition, highlighting the existence of factors that induce microbial adaptations in each location. Functional gut microbiome analyses revealed its role in the biosynthesis and degradation of vitamins, cofactors, proteinogenic amino acids, carbohydrates, nucleosides and nucleotides, fatty acids, lipids, and other compounds necessary for the marine iguanas. The overall bacterial ARG abundance was relatively low (0.006%); nevertheless, the presence of genes encoding resistance to 22 drug classes was identified in the iguana's gut metagenome. ARG-carrying contig and co-occurrence network analyses revealed that commensal bacteria are the main hosts of ARGs. Taxa of public health interest such as Salmonella, Vibrio, and Klebsiella also carried multidrug-resistance genes associated with MGEs which can influence the dissemination of ARGs through horizontal gene transfer.ConclusionMarine iguanas depend on the gut microbiome for the biosynthesis and degradation of several compounds through a symbiotic relationship. Niche-specific adaptations were evidenced in the pool of microbial accessory genes (i.e., ARGs, MGEs, and virulence) and metabolic pathways, but not in the microbiome composition. Culture-independent approaches outlined the presence of a diverse resistome composition in the Galapagos marine iguanas from remote islands. The presence of AR pathogens in marine iguanas raises concerns about the dispersion of microbial-resistant threats in pristine areas, highlighting wildlife as sentinel species to identify the impact of AU.

Project description:The Galápagos Archipelago is home to a diverse range of marine bioregions due to the confluence of several cold and warm water currents, resulting in some of the most productive tropical marine ecosystems in the world. These ecosystems are strongly influenced by El Niño events which can reduce primary production by an order of magnitude, dramatically reducing energy available throughout the food web. Fisheries are an important component of the local economy, although artisanal and illegal overfishing have dramatically reduced the productivity of invertebrate and finfish resources in recent decades, resulting in reductions in catches for local fishers. The regionally-endemic sailfin grouper (Myctereoperca olfax), locally known as bacalao, was once the most important fished species in the Galápagos, but is now listed as vulnerable by the IUCN due to its limited range and dramatic declines in catch over time. It is unknown how reduction of this predatory species has affected ecosystem structure and function. In the absence of stock assessments, we used an estimate of unfished bacalao biomass from fishers' ecological knowledge along with unfished biomass estimates of other heavily exploited stocks-lobster (Panulirus penicillatus and P. gracilis) and sea cucumber (Isostichopus fuscus)-to create historical, unfished versions of existing modern day ecosystem models. We used the unfished and modern versions of the ecosystem models to test the ecosystem effects of bacalao exploitation at the Bolivar Channel, located in the cold, west upwelling bioregion of the archipelago during both El Niño and non El Niño years, and at Floreana Island, in the warmer, central bioregion. Fishers' ecological knowledge indicates that at present, the biomass of bacalao is at least seven times lower than when unfished. This reduced bacalao biomass is linked with a greatly reduced ecosystem role compared to when unfished, and ecosystem role is further reduced in El Niño years. Allowing bacalao populations to rebuild to at least half of unfished biomass would partially restore their role within these ecosystems, while also resulting in greater fisheries catches. Comparing ecosystem impacts caused by fishing and El Niño, fishing has had a greater negative impact on bacalao ecosystem role than regular El Niño events.

Project description:Parasitism is among the most common forms of coexistence of organisms of different species. Hemoparasites live in the bloodstream of the host where they complete different life-cycle stages. Members of the phylum Apicomplexa constitute a large portion of all hemoparasites infecting reptiles and their parasite transmitting vectors, including arthropods. In this study, we carried out a survey and molecular identification of hemoparasites in blood samples of the iconic Galápagos marine iguana (Amblyrhynchus cristatus). Major island populations of marine iguanas were sampled to examine large-scale biogeographic patterns of parasite diversity and prevalence. Nested PCRs were used to amplify segments of the 18S rRNA-gene of hemoparasites. Furthermore, ticks attached to marine iguanas were collected and analyzed in the same way to assess their potential use as a non-invasive method for the detection of hemoparasites in vertebrate host species. PCR products were sequenced and a phylogenetic analysis was carried out showing the presence of two genetically distinct clusters of hemoparasites, one more commonly distributed than the other one, belonging to the genera Hepatozoon and/or Hemolivia (Apicomplexa: Eucoccidiorida). Overall, 25% of marine iguanas were infected by hemoparasites. However, infection rates varied strongly among particular island populations (from 3.45% to 50%). Although marine iguanas are an extremely mobile species that has colonized all islands in the Galápagos archipelago, parasite occurrence was not related to geographical distance, suggesting that dispersal behavior has a minor role in parasite transmission. On most islands, females tended to have higher infection rates than males, but this relationship was only significant on one island. Overall, ticks and marine iguanas had similar prevalence and diversity of parasites. However, the infection profiles of ticks and their corresponding hosts (marine iguanas) did not mirror one another, indicating that this method cannot be used reliably to assess marine iguana infection status. Interestingly, we found that hemoparasite prevalence in marine iguanas and ticks tended to be positively correlated across islands. Our results indicate that certain populations of marine iguanas may have special mechanisms and adaptations to cope with parasite infection. In addition, other factors such as vector density, anthropogenic-related activities or the immunological state of marine iguanas could potentially affect the striking variation in hemoparasite prevalence across island populations.

Project description:BackgroundMarine iguanas (Amblyrhynchus cristatus) inhabit the coastlines of large and small islands throughout the Galápagos archipelago, providing a rich system to study the spatial and temporal factors influencing the phylogeographic distribution and population structure of a species. Here, we analyze the microevolution of marine iguanas using the complete mitochondrial control region (CR) as well as 13 microsatellite loci representing more than 1200 individuals from 13 islands.ResultsCR data show that marine iguanas occupy three general clades: one that is widely distributed across the northern archipelago, and likely spread from east to west by way of the South Equatorial current, a second that is found mostly on the older eastern and central islands, and a third that is limited to the younger northern and western islands. Generally, the CR haplotype distribution pattern supports the colonization of the archipelago from the older, eastern islands to the younger, western islands. However, there are also signatures of recurrent, historical gene flow between islands after population establishment. Bayesian cluster analysis of microsatellite genotypes indicates the existence of twenty distinct genetic clusters generally following a one-cluster-per-island pattern. However, two well-differentiated clusters were found on the easternmost island of San Cristóbal, while nine distinct and highly intermixed clusters were found on youngest, westernmost islands of Isabela and Fernandina. High mtDNA and microsatellite genetic diversity were observed for populations on Isabela and Fernandina that may be the result of a recent population expansion and founder events from multiple sources.ConclusionsWhile a past genetic study based on pure FST analysis suggested that marine iguana populations display high levels of nuclear (but not mitochondrial) gene flow due to male-biased dispersal, the results of our sex-biased dispersal tests and the finding of strong genetic differentiation between islands do not support this view. Therefore, our study is a nice example of how recently developed analytical tools such as Bayesian clustering analysis and DNA sequence-based demographic analyses can overcome potential biases introduced by simply relying on FST estimates from markers with different inheritance patterns.

Project description:BackgroundChemical signals are widely used in the animal kingdom, enabling communication in various social contexts, including mate selection and the establishment of dominance. Femoral glands, which produce and release waxy secretions into the environment, are organs of central importance in lizard chemical communication. The Galápagos marine iguana (Amblyrhynchus cristatus) is a squamate reptile with a lek-mating system. Although the lekking behaviour of marine iguanas has been well-studied, their potential for sexual communication via chemical cues has not yet been investigated. Here we describe the diversity of the lipophilic fraction of males' femoral gland secretions among 11 island populations of marine iguanas, and compare it with the composition of its sister species, the Galápagos land iguana (Conolophus subcristatus). We also conducted behavioural observations in marine iguana territorial males in order to explore the possible function of these substances in the context of male dominance in leks.MethodsFemoral secretions were analysed by gas chromatography coupled to mass spectrometry (GC-MS), and chromatography with a flame ionisation detector (GC-FID) in order to characterise the lipophilic composition. To understand the potential role of femoral secretions in marine iguana intraspecific communication, territorial males were sampled for their femoral glands and monitored to record their head bob rate-a territorial display behaviour in males-as well as the number of females present in their leks.ResultsWe found that the gland secretions were composed of ten saturated and unsaturated carboxylic acids ranging in chain length between C16 and C24, as well as three sterols. Cholesterol was the main compound found. Intriguingly, land iguanas have a higher diversity of lipophilic compounds, with structural group of lipids (i.e. aldehydes) entirely absent in marine iguanas; overall the chemical signals of both species were strongly differentiated. Lipid profiles also differed among populations of marine iguanas from different islands, with some islands demonstrating a high diversity of lipophilic compounds (i.e. full spectra of compounds), and others lacking one or more compounds. Among the compounds most frequently found missing were 11- and 13-eicosenoic acids. Gland secretions of males with a better body condition and with a higher dominance status (i.e. those accompanied by females and with higher head bob display) were proportionately richer in C20-unsaturated fatty acids (11-eicosenoic acid).DiscussionLand and marine iguanas strongly diverged in their chemical composition of the femoral glands likely due to ecological differences between both species. Despite that marine iguana populations varied in their femoral gland composition that was not related to their genetic structure. Our results indicated that 11-eicosenoic acid may play an important role in intraspecific chemical communication in marine iguanas.

Dataset Information

No impact of a short-term climatic "El Nino" fluctuation on gut microbial diversity in populations of the Galapagos marine iguana (Amblyrhynchus cristatus).

Publications

No impact of a short-term climatic "El Niño" fluctuation on gut microbial diversity in populations of the Galápagos marine iguana (Amblyrhynchus cristatus).

Similar Datasets

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