bioRxiv

Abstract

Multicellularity evolved multiple times independently during eukaryotic diversification. Two distinct mechanisms underpin multicellularity: clonal development (serial cell division of a
single precursor cell) and aggregation (in which independent cells assemble into a multicellular entity). Clonal and aggregative development are traditionally considered to be mutually exclusive and to result from independent acquisitions of multicellularity. Here, we show that the choanoflagellate Choanoeca flexa, a close relative of animals that forms contractile monolayers of cells (or “sheet colonies”), develops by an unconventional intermediate mechanism that we name “clonal-aggregative multicellularity”. We find that C. flexa sheets can form through purely clonal processes, purely aggregative processes, or a combination of both, depending on experimental conditions. To assess the ecological relevance of these findings, we characterize the natural context of multicellular development in the native environment of C. flexa on the island of Curaçao. We show that the C. flexa life cycle is environmentally regulated by extreme salinity fluctuations in splash pools undergoing cycles of evaporation and refilling. Upon desiccation, C. flexa colonies dissociate into drought resistant quiescent cells, which resume activity and reform multicellular sheets after rehydration. We hypothesize that clonal-aggregative development reflects selection for fast transitions into and out of multicellularity in the ephemeral context of coastal splash pools. Our findings underscore the potential of the exploration of biodiversity for revealing new fundamental biological phenomena and expand the known option space for both multicellular development and for the origin of animal multicellularity.

Abstract

The mangrove-seagrass-coral reef continuum is of immense ecological and socio-economic importance, supporting biodiversity, carbon storage, coastal protection, fisheries, and tourism. The presence of extreme environmental conditions along this continuum could support adaptive refugia for climate-sensitive taxa such as reef-building corals but physicochemical conditions are rarely assessed at sufficient spatiotemporal resolution. Furthermore, coastal development and low water quality increasingly threaten these interconnected coastal ecosystems. Yet, time-integrated pollution monitoring is absent at most locations. Here, we used a multi-disciplinary approach to assess benthic cover, coral diversity, and >20 abiotic parameters characterizing two mangrove- and seagrass-dominated inland bays and two nearby coral reefs in Curaçao (southern Caribbean) during the cool, dry season and warm, wet season. This was combined with time-integrated pollution monitoring using bioindicators to assess nutrients and trace metal pollution (inland bays only), and passive samplers and bioassays to assess organic chemical pollution (all four sites) during the wet season. This approach revealed a previously undocumented extent of strong diel and seasonal environmental variability in the two inland bays, with temperature, pH and dissolved oxygen frequently reaching values predicted under moderate-to-severe future climate scenarios. In addition, the inland bays had greater nutrient concentrations (especially ammonium) and ecotoxicological risks than the nearby reefs during the wet season due to run-off, industrial- and wastewater effluents, ports and boating. Overall, our findings show that Curaçao’s inland bays have significant potential to serve as natural laboratories to study the effects of future ocean conditions on resident taxa in situ. This however applies within the context of strong diel fluctuations and with the caveat of co-occurring stressors. Our work confirms the important role of mangrove and seagrass habitats as resilience hotspots for climate-sensitive taxa but also highlights the urgent need to improve monitoring, water quality and protection of these valuable habitats along the mangrove-seagrass-coral reef continuum.

Genome size is a fundamental biological trait that is known to exhibit high diversity among eukaryotic species, but its intraspecific diversity has only scarcely been studied to date. In scleractinian corals, genome size data are only available for a few species. In this study, intra- and interspecific variations in genome size of the coral genus Agaricia collected from Curaçao were investigated. Morphology was congruent with genetic analyses of the nuclear markers internal transcribed spacer 2 (ITS2) and L-threonine 3-dehydrogenase (TDH) in delimiting three Agaricia species among our samples. A refined Feulgen Image Analysis Densitometry (FIAD) protocol yielded genome sizes that ranged from 0.359 pg to 0.593 pg within this genus (a 1.7-fold range). The highest intraspecific variation in genome size was recorded in the depth-generalist A. lamarcki (1.5-fold range), followed by the depth specialist A. humilis (1.4-fold range) and A. agaricites (1.3-fold range), the species with an intermediate depth distribution. The mean genome size of A. agaricites (0.495 pg) was significantly larger than that of A. lamarcki (0.448 pg) and A. humilis (0.434 pg). No correlation between average genome size and nucleotide polymorphism π was detected, but we found an almost linear correlation between intraspecific variance of genome size and π of ITS2 (Pearson’s r = 0.984, p = 0.113). Genome size and collection depths of both A. lamarcki (Pearson’s r = 0.328, p = 0.058) and A. agaricites (Pearson’s r = -0.270, p = 0.221) were also not significantly associated. To our knowledge, this study provides the first account of intraspecific variation in corals; the apparent correlation detected between the nucleotide polymorphism of a species and the variance of its genome size will have to be tested using a larger taxonomic spectrum of scleractinian corals as well as in other groups of animals.

Abstract  Evolutionary tradeoffs between life-history strategies are central to animal evolution. However, because microbes can influence aspects of host physiology, behavior, and resistance to stress or disease, changes in animal-microbial symbioses have the potential to mediate life-history tradeoffs. Scleractinian corals provide a highly biodiverse and data-rich host system to test this idea, made more relevant by increases in coral disease outbreaks as a result of anthropogenic changes to climate and reef ecosystems. Identifying factors that determine coral disease susceptibility has therefore become a focus for reef conservation efforts. Using a comparative approach, we tested if coral microbiomes correlate with disease susceptibility across 425 million years of coral evolution by combining a cross-species coral microbiome survey (the “Global Coral Microbiome Project”) with long-term disease prevalence data at multiple sites. Interpreting these data in their phylogenetic context, we show that microbial dominance and composition predict disease susceptibility. We trace this dominance-disease association to a single putatively beneficial bacterial symbiont, Endozoicomonas, whose relative abundance in coral tissue explained 30% of variation in disease susceptibility and 60% of variation in microbiome dominance across 40 coral genera. Conversely, Endozoicomonas abundances in coral tissue strongly correlated with high growth rates. These results demonstrate that the evolution of microbial symbiosis in corals correlates with both disease prevalence and growth rate. Exploration of the mechanistic basis for these findings will be important for our understanding of how microbial symbiosis influences animal life-history tradeoffs, and in efforts to use microbes to increase coral growth or disease resistance in-situ. 

Abstract  

Tropical reef-building corals exist in intimate symbiosis with diverse microbes and viruses. Coral microbiomes are generally much less diverse than their environment, but across studied corals, the biodiversity of these microbiomes varies greatly. It has previously been hypothesized that differences in coral innate immunity in general, and the copy number of TIR-domain containing innate immune genes in particular, may drive interspecific differences in microbiome structure. Despite many existing studies of coral microbiomes, this hypothesis has previously been difficult to test due to a lack of consistently collected cross-species data on coral microbiomes. In this manuscript, we reannotate TIR-domain containing genes across diverse coral genomes, and use phylogenetic comparative methods to compare these innate immune gene copy numbers against 16S rRNA marker gene data on coral mucus, tissue, and skeleton microbiomes from the Global Coral Microbiome Project (GCMP). The copy number of Toll-like receptor (TLRs) and Interleukin-1 receptor (IL-1Rs) gene families, as well as the total genomic count of their constituent domains (LRR and TIR domains; and Ig and TIR domains, respectively), explained most interspecific differences in microbiome richness and beta-diversity among corals with sequenced genomes. We find that these correlations are also anatomically specific, with an especially strong correlation between IL-1R gene copy numbers and microbiome richness in the coral’s endolithic skeleton. Together, these results suggest innate immunity may play a key role in sculpting microbiome structure in corals. 

ABSTRACT

A major challenge in invasion ecology is determining which introduced species pose a threat to resident species through competitive displacement. Here, we provide a statistical framework rooted in coexistence theory to calculate coexistence outcomes – including competitive displacement – between resident and invading species. Advantageously, our framework uses readily available trait and abundance data rather than the demographic data traditionally used in coexistence theory applications which is often difficult to collect for most species. Our framework provides methods for predicting displacement that has yet to manifest in incipient invasions, and for quantifying displacement in ongoing invasions. We apply this framework to the native and introduced gecko species on Curaçao and predict the displacement of all three native species by introduced species and quantify that the displacement of one native species is already underway. Our results affirm that trait and abundance data are suitable proxies to reasonably predict and quantify coexistence outcomes. 

Abstract.– Intraspecific diversity is among the most important biological variables, although still poorly understood for most species. Iguana iguana is a Neotropical lizard known from Central and South America, including from numerous Caribbean islands. Despite the presence of native melanistic I. iguana populations in the Lesser Antilles, these have received surprisingly little research attention. Here we assessed population size, distribution, degree of melanism, and additional morphological and natural history characteristics for the melanistic iguanas of Saba, Caribbean Netherlands based on a one-month fieldwork visit. Using Distance sampling from a 38- transect dataset we estimate the population size at 8233 ±2205 iguanas. Iguanas mainly occurred on the southern and eastern sides of the island, between 180-390 m (max altitude 530 m), with highest densities both in residential and certain natural areas. Historically, iguanas were relatively more common at higher altitudes, probably due to more extensive forest clearing for agricultural reasons. No relationship was found between the degree of melanism and elevation, and few animals were completely melanistic. Furthermore, we found that body-ratio data collection through photographs is biased and requires physical measuring instead. Although the population size appears larger than previously surmised, the limited nesting sites and extremely low presence of juvenile and hatchling iguanas (2.4%), is similarly worrying as the situation for I. delicatissima on neighboring St. Eustatius. The island’s feral cat and large goat population are suspected to impact nest site quality, nest success, and hatchling survival. These aspects require urgent future research to guide necessary conservation management.

We estimated occupancy, abundance (lambda), detection probability, density/ha and abundance of a regionally endemic snake in the Colubrid family on the Dutch Caribbean island of Saba in 2021, four years after hurricanes Irma and Maria impacted the island. Line transect surveys were conducted at 74 sites covering 6.7 ha. The proportion of sites occupied was estimated at 0.74 (min 0.48, max 0.90), with occupancy varying between vegetation types and across elevational gradients. Similarly, lambda was estimated at 1.61 (min 0.7, max 3.7) but varied between vegetation types and elevational gradients. Detection probability was estimated at 0.15 (min 0.10, max 0.21). Using Distance sampling, we estimated 10.9 (min 7.3, max 16.2) racers/ha, with a total population estimate of 4,917 (min 2,577, max 6,362) across the entire study region (438.6 ha.) Based on anecdotal observations from Saban residents and prior literature describing the pre-hurricane population as “abundant” (at least 2.0 racers/hour), we posit that the population experienced a hurricane-induced decline but may have since recovered, though not to previous levels (1.28 racers/hour). Nevertheless, our results suggest that racer densities on Saba are currently higher than those on St. Eustatius. Despite this, given the species’ extremely limited extant range and the presence of invasive species on both islands, prevention of local extirpation should be a high conservation priority.

ABSTRACT

Catastrophic events, like hurricanes, bring lethal conditions that can have population-altering effects. The threatened Caribbean dry forest occurs in a region known for its high-intensity hurricane seasons and high species endemism, highlighting the necessity to better understand hurricane impacts as fragmentation and clearing of natural habitat continues. However, such studies remain rare, and for reptiles are mostly restricted to Anolis. Here we used single-season occupancy modeling to infer the impact of the intense 2017 Atlantic hurricane season on the critically endangered Lesser Antillean Iguana, Iguana delicatissima. We surveyed 30 transects across eight habitats on St. Eustatius during 2017-2019, which resulted in 344 individual surveys and 98 iguana observations. Analyses of abundance and site occupancy indicated both measures for 2018 and 2019 were strongly reduced compared to the pre-hurricane 2017 state. Iguanas at higher elevations were affected more profoundly, likely due to higher wind speeds, tree damage and extensive defoliation. Overall, our results indicate a decrease in population estimates (23.3-26.5%) and abundance (22-23.8%) for 2018 and 2019, and a 75% reduction in the number of opportunistic sightings of tagged iguanas between 2017-2018. As only small and isolated I. delicatissima populations remain, our study further demonstrates their vulnerability to stochastic events. Considering the frequency and intensity of hurricanes are projected to increase, our results stress the urgent need for population-increasing conservation actions in order to secure the long-term survival of I. delicatissima throughout its range.

Abstract

We estimated population densities of the red-bellied racer (Alsophis rufiventris) on the Caribbean island of St. Eustatius in 2011, 2018 and 2019 to determine the likely influence of hurricanes Irma and Maria (September 2017), in addition to evaluating abiotic parameters which may be correlated with its presence. Surveys were conducted at seven sites in 2011 prior to the hurricanes, and at 81 and 108 sites in 2018 and 2019 respectively posterior to the hurricanes. A total of 8.2 ha was surveyed in 2011, and 11.42 ha in 2018/2019. The pre-hurricane (2011) racer density estimate was 9.2/ha (min 7.3 - max 11.6); post-hurricane estimates were 4.6/ha (min 3.4 - max 6.0) in 2018 and 5.0/ha (min 3.8 - max 6.5) in 2019. The pre-hurricane encounter rate of individual racers was 16.0 snakes/hour compared to 0.34 snakes/hour in 2018 and 0.41 snakes/hour in 2019 (post-hurricane). The decrease in encounter rates between 2011 and 2019 implies a negative impact of the hurricanes on racer abundance. Based on calculations of detection probability (0.02 in 2018 and 0.03 in 2019), post-hurricane lambda estimates were 1.82 (95% CI 0.66 - 5.01) in 2018 and 1.60 (95% CI 0.39 - 6.65) snakes/ha in 2019. Given the current small size of the remaining population and the presence of invasive species across the snake’s range, this species could be at risk of local extirpation. We suggest conservation actions such as invasive species management and habitat restoration to enable further recovery.