Evolution and environment of Caribbean coastal ecosystems.

Isolation of the Caribbean Sea from the tropical Eastern Pacific by uplift of the Isthmus of Panama in the late Pliocene was associated with major, taxonomically variable, shifts in Caribbean biotic composition, and extinction, but inferred causes of these biological changes have remained elusive. We addressed this through falsifiable hypotheses about how independently determined historical changes in oceanographic conditions may have been responsible. The most striking environmental change was a sharp decline in upwelling intensity as measured from decreases in intra-annual fluctuations in temperature and consequently in planktonic productivity. We then hypothesized three general categories of biological response based upon observed differences in natural history between the oceans today. These include changes in feeding ecology, life histories, and habitats. As expected, suspension feeders and predators became rarer as upwelling declined. However, predicted increases in benthic productivity by reef corals, and benthic algae were drawn out over more than 1 Myr as seagrass and coral reef habitats proliferated; a shift that was itself driven by declining upwelling. Similar time lags occurred for predicted shifts in reproductive life history characteristics of bivalves, gastropods, and bryozoans. Examination of the spatial variability of biotic change helps to understand the time lags. Many older species characteristic of times before environmental conditions had changed tended to hang on in progressively smaller proportions of locations until they became extinct as expected from metapopulation theory and the concept of extinction debt. Faunal turnover may not occur until a million or more years after the environmental changes ultimately responsible.

Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution.

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host's physiological capacities; however, the identity and functional role(s) of key members of the microbiome ("core microbiome") in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems' capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts' plastic and adaptive responses to environmental change requires (i) recognizing that individual host-microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

Fossil dermal denticles reveal the preexploitation baseline of a Caribbean coral reef shark community.

Preexploitation shark baselines and the history of human impact on coral reef-associated shark communities in the Caribbean are tpoorly understood. We recovered shark dermal denticles from mid-Holocene (∼7 ky ago) and modern reef sediments in Bocas del Toro, Caribbean Panama, to reconstruct an empirical shark baseline before major human impact and to quantify how much the modern shark community in the region had shifted from this historical reference point. We found that denticle accumulation rates, a proxy for shark abundance, declined by 71% since the mid-Holocene. All denticle morphotypes, which reflect shark community composition, experienced significant losses, but those morphotypes found on fast-swimming, pelagic sharks (e.g., families Carcharhinidae and Sphyrnidae) declined the most. An analysis of historical records suggested that the steepest decline in shark abundance occurred in the late 20th century, coinciding with the advent of a targeted shark fishery in Panama. Although the disproportionate loss of denticles characterizing pelagic sharks was consistent with overfishing, the large reduction in denticles characterizing demersal species with low commercial value (i.e., the nurse shark Ginglymostoma cirratum) indicated that other stressors could have exacerbated these declines. We demonstrate that the denticle record can reveal changes in shark communities over long ecological timescales, helping to contextualize contemporary abundances and inform shark management and ecology.

Mercury Pollution History in Tropical and Subtropical American Lakes: Multiple Impacts and the Possible Relationship with Climate Change.

Sediment cores obtained from 11 tropical and subtropical American lakes revealed that local human activities significantly increased mercury (Hg) inputs and pollution levels. Remote lakes also have been contaminated by anthropogenic Hg through atmospheric depositions. Long-term sediment-core profiles revealed an approximately 3-fold increase in Hg fluxes to sediments from c. 1850 to 2000. Generalized additive models indicate that c. 3-fold increases in Hg fluxes also occurred since 2000 in the remote sites, while Hg emissions from anthropogenic sources have remained relatively stable. The tropical and subtropical Americas are vulnerable to extreme weather events. Air temperatures in this region have shown a marked increase since the 1990s, and extreme weather events arising from climate change have increased. When comparing Hg fluxes to recent (1950-2016) climatic changes, results show marked increases in Hg fluxes to sediments during dry periods. The Standardized Precipitation-Evapotranspiration Index (SPEI) time series indicate a tendency toward more extreme drier conditions across the study region since the mid-1990s, suggesting that instabilities in catchment surfaces caused by climate change are responsible for the elevated Hg flux rates. Drier conditions since c. 2000 appear to be promoting Hg fluxes from catchments to lakes, a process that will likely be exacerbated under future climate-change scenarios.

Host-associated microbiomes drive structure and function of marine ecosystems.

The significance of symbioses between eukaryotic hosts and microbes extends from the organismal to the ecosystem level and underpins the health of Earth's most threatened marine ecosystems. Despite rapid growth in research on host-associated microbes, from individual microbial symbionts to host-associated consortia of significantly relevant taxa, little is known about their interactions with the vast majority of marine host species. We outline research priorities to strengthen our current knowledge of host-microbiome interactions and how they shape marine ecosystems. We argue that such advances in research will help predict responses of species, communities, and ecosystems to stressors driven by human activity and inform future management strategies.

Isotopes from fossil coronulid barnacle shells record evidence of migration in multiple Pleistocene whale populations.

Migration is an integral feature of modern mysticete whale ecology, and the demands of migration may have played a key role in shaping mysticete evolutionary history. Constraining when migration became established and assessing how it has changed through time may yield valuable insight into the evolution of mysticete whales and the oceans in which they lived. However, there are currently few data which directly assess prehistoric mysticete migrations. Here we show that calcite δ18O profiles of two species of modern whale barnacles (coronulids) accurately reflect the known migration routes of their host whales. We then analyze well-preserved fossil coronulids from three different locations along the eastern Pacific coast, finding that δ18O profiles from these fossils exhibit trends and ranges similar to modern specimens. Our results demonstrate that migration is an ancient behavior within the humpback and gray whale lineages and that multiple Pleistocene populations were undertaking migrations of an extent similar to those of the present day.

Marine extinction risk shaped by trait-environment interactions over 500 million years.

Perhaps the most pressing issue in predicting biotic responses to present and future global change is understanding how environmental factors shape the relationship between ecological traits and extinction risk. The fossil record provides millions of years of insight into how extinction selectivity (i.e., differential extinction risk) is shaped by interactions between ecological traits and environmental conditions. Numerous paleontological studies have examined trait-based extinction selectivity; however, the extent to which these patterns are shaped by environmental conditions is poorly understood due to a lack of quantitative synthesis across studies. We conducted a meta-analysis of published studies on fossil marine bivalves and gastropods that span 458 million years to uncover how global environmental and geochemical changes covary with trait-based extinction selectivity. We focused on geographic range size and life habit (i.e., infaunal vs. epifaunal), two of the most important and commonly examined predictors of extinction selectivity. We used geochemical proxies related to global climate, as well as indicators of ocean acidification, to infer average global environmental conditions. Life-habit selectivity is weakly dependent on environmental conditions, with infaunal species relatively buffered from extinction during warmer climate states. In contrast, the odds of taxa with broad geographic ranges surviving an extinction (>2500 km for genera, >500 km for species) are on average three times greater than narrow-ranging taxa (estimate of odds ratio: 2.8, 95% confidence interval = 2.3-3.5), regardless of the prevailing global environmental conditions. The environmental independence of geographic range size extinction selectivity emphasizes the critical role of geographic range size in setting conservation priorities.

Evidence of size-selective evolution in the fighting conch from prehistoric subsistence harvesting.

Intensive size-selective harvesting can drive evolution of sexual maturity at smaller body size. Conversely, prehistoric, low-intensity subsistence harvesting is not considered an effective agent of size-selective evolution. Uniting archaeological, palaeontological and contemporary material, we show that size at sexual maturity in the edible conch Strombus pugilis declined significantly from pre-human (approx. 7 ka) to prehistoric times (approx. 1 ka) and again to the present day. Size at maturity also fell from early- to late-prehistoric periods, synchronous with an increase in harvesting intensity as other resources became depleted. A consequence of declining size at maturity is that early prehistoric harvesters would have received two-thirds more meat per conch than contemporary harvesters. After exploring the potential effects of selection biases, demographic shifts, environmental change and habitat alteration, these observations collectively implicate prehistoric subsistence harvesting as an agent of size-selective evolution with long-term detrimental consequences. We observe that contemporary populations that are protected from harvesting are slightly larger at maturity, suggesting that halting or even reversing thousands of years of size-selective evolution may be possible.

RADReef: A global Holocene Reef Rate of Accretion Dataset.

Reef cores are a powerful tool for investigating temporal changes in reef communities. Radiometric dating facilitates the determination of vertical accretion rates, which has allowed for examination of local-regional controlling factors, such as subsidence and sea level changes. Coral reefs must grow at sufficient rates to keep up with sea level rise, or risk 'drowning.' As sea level is expected to rise significantly in the next 100 years and beyond, it is important to understand whether reefs will be able to survive. Historical records of reef accretion rates extracted from cores provide valuable insights into extrinsic controlling factors of reef growth and are instrumental in helping predict if future reefs can accrete at rates needed to overcome predicted sea level changes. While extensive research exists at local and regional scales, limited attention has been given to identifying global patterns and drivers. To address this, we present "RADReef": A global dataset of dated Holocene reef cores. RADReef serves as a foundation for further research on past, present and future reef accretion.

[Environmental response in the Pacific to aseismic Cocos Ridge subduction (Panama and Costa Rica)]. / Respuesta ambiental en el pacífico frente a la subducción de la dorsal asísmica de Cocos (Panamá y Costa Rica).

The evolution of the marine communities along the Pacific coast of Central America, may have changed in response to the formation of the Isthmus of Panama. To evaluate the effect of the Aseismic Cocos Ridge (DAC) subduction on the marine benthic communities, we reconstructed benthic assemblages from Neogene fossiliferous formations in Burica and Nicoya peninsulas of Panama and Costa Rica. Paleoecological and paleoenvironmental conditions were reconstructed by comparing community structure from bulk fossil samples with dredge collections from modern Tropical American seas, using principal component analysis. Our results indicate that during the early Pliocene, before the closing of the Isthmus, some oceanic islands existed with moderate upwelling in the Burica region. After the closure, during the late Pliocene and early Pleistocene the collision of the DAC caused an uplift of the seafloor, where water depth of 2 300m became shallow waters of less than 40m depth. Meanwhile, upwelling intensified in the open ocean the uplift that had formed small islands in coastal areas of Burica, creating protected areas and limiting the upwelling effect that was given in open ocean. The subduction of the DAC continued until the islands were joined to the mainland and gradually disappeared, allowing the return of the upwelling. During the middle Pleistocene a second process of accelerated uplift with speeds of 8m/1000 years provoked again the elevation of the seafloor and later the elevation of the Talamanca Range. The new range formed a barrier that blocked the passage of the Trade winds, created new ecological conditions and optimized and allowed the growth of the best coral reefs in the coasts of the tropical Eastern Pacific (POT) between Panama and Costa Rica.

Pleistocene sea level changes and crocodile population histories on the Isthmus of Panama: A comment on Avila-Cervantes et al. (2020).

Avila-Cervantes et al. proposed that glacial-interglacial sea level changes played an important role in the evolutionary and demographic histories of the crocodile Crocodylus acutus on the Isthmus of Panama. However, the study used erroneous sea level proxy data that produced flawed paleogeographic reconstructions. We present new paleogeographic reconstructions and review the timing of, and proposed mechanisms behind, the demographic events estimated by Avila-Cervantes et al.. With the data currently available, we find little evidence to support the hypothesis that sea level changes drove population demographic events in crocodiles on the Isthmus. Alternative hypotheses, including changing climate and habitat suitability, are equally valid and should be considered along with well-supported sea level models.

Unprecedented frequency of mitochondrial introns in colonial bilaterians.

Animal mitogenomes are typically devoid of introns. Here, we report the largest number of mitochondrial introns ever recorded from bilaterian animals. Mitochondrial introns were identified for the first time from the phylum Bryozoa. They were found in four species from three families (Order Cheilostomatida). A total of eight introns were found in the complete mitogenome of Exechonella vieirai, and five, 17 and 18 introns were found in the partial mitogenomes of Parantropora penelope, Discoporella cookae and Cupuladria biporosa, respectively. Intron-encoded protein domains reverse transcriptase and intron maturase (RVT-IM) were identified in all species. Introns in E. vieirai and P. penelope had conserved Group II intron ribozyme domains V and VI. Conserved domains were lacking from introns in D. cookae and C. biporosa, preventing their further categorization. Putative origins of metazoan introns were explored in a phylogenetic context, using an up-to-date alignment of mitochondrial RVT-IM domains. Results confirmed previous findings of multiple origins of annelid, placozoan and sponge RVT-IM domains and provided evidence for common intron donor sources across metazoan phyla. Our results corroborate growing evidence that some metazoans with regenerative abilities (i.e. placozoans, sponges, annelids and bryozoans) are susceptible to intron integration, most likely via horizontal gene transfer.

Modern, archaeological, and paleontological DNA analysis of a human-harvested marine gastropod (Strombus pugilis) from Caribbean Panama.

Although protocols exist for the recovery of ancient DNA from land snail and marine bivalve shells, marine conch shells have yet to be studied from a paleogenomic perspective. We first present reference assemblies for both a 623.7 Mbp nuclear genome and a 15.4 kbp mitochondrial genome for Strombus pugilis, the West Indian fighting conch. We next detail a method to extract and sequence DNA from conch shells and apply it to conch from Bocas del Toro, Panama across three time periods: recently-eaten and discarded (n = 3), Late Holocene (984-1258 before present [BP]) archaeological midden (n = 5), and mid-Holocene (5711-7187 BP) paleontological fossil coral reef (n = 5). These results are compared to control DNA extracted from live-caught tissue and fresh shells (n = 5). Using high-throughput sequencing, we were able to obtain S. pugilis nuclear sequence reads from shells across all age periods: up to 92.5 thousand filtered reads per sample in live-caught shell material, 4.57 thousand for modern discarded shells, 12.1 thousand reads for archaeological shells, and 114 reads in paleontological shells. We confirmed authenticity of the ancient DNA recovered from the archaeological and paleontological shells based on 5.7× higher average frequency of deamination-driven misincorporations and 15% shorter average read lengths compared to the modern shells. Reads also mapped to the S. pugilis mitochondrial genome for all but the paleontological shells, with consistent ratios of mitochondrial to nuclear mapped reads across sample types. Our methods can be applied to diverse archaeological sites to facilitate reconstructions of the long-term impacts of human behaviour on mollusc evolutionary biology.

A century of limnological evolution and interactive threats in the Panama Canal: Long-term assessments from a shallow basin.

Large tropical river dam projects are expected to accelerate over the forthcoming decades to satisfy growing demand for energy, irrigation and flood control. When tropical rivers are dammed the immediate impacts are relatively well studied, but the long-term (decades-centuries) consequences of impoundment remain poorly known. We combined historical records of water quality, river flow and climate with a multi-proxy (macrofossils, diatoms, biomarkers and trace elements) palaeoecological approach to reconstruct the limnological evolution of a shallow basin in Gatun Lake (Panama Canal, Panama) and assess the effects of multiple linked factors (river damming, forest flooding, deforestation, invasive species, pollution and hydro-climate) on the study area. Results show that a century after dam construction, species invasion, deforestation and salt intrusions have forced a gradual change in the study basin from a swamp-type environment towards a more saline lake-governed system of benthic-littoral production likely associated with the expansion of macrophyte stands. Hydrology still remains the most important long-term (decades) structural factor stimulating salinity intrusions, primary productivity, deposition of minerals, and reduction of water transparency during wet periods. During dry periods, physical-chemical conditions are in turn linked to clear water and aerobic conditions while nutrients shift to available forms for the aquatic biota in the detrital-rich reductive sediments. Our study suggests that to preserve the natural riverine system functioning of this area of the Panama Canal, management activities must address long-term ecosystem structural drivers such as river flow, runoff patterns and physical-chemical conditions.

Defining variation in pre-human ecosystems can guide conservation: An example from a Caribbean coral reef.

Many Caribbean coral reefs are heavily degraded, yet their pre-human, natural states are often assumed or estimated using space-for-time substitution approaches. Here we use an 11-hectare suite of fossilised mid-Holocene (7.2-5.6 ka) fringing reefs in Caribbean Panama to define natural variation in hard coral community structure before human-impact to provide context to the states of the same reefs today. We collected bulk samples from four trenches dug into the mid-Holocene fossil reef and surficial bulk samples from 2-10 m depths on five adjacent modern reefs extending over 5 km. Analysis of the abundances of coral taxa in fossil bulk samples define the Historical Range of Variation (HRV) in community structure of the reefs. When compared to the community structure of adjacent modern reefs, we find that most coral communities today fall outside the HRV, identifying them as novel ecosystems and corroborating the well-documented transition from acroporid-dominated Caribbean reefs to reefs dominated by stress-tolerant taxa (Porites and Agaricia). We find one modern reef, however, whose community composition remains within the HRV showing that it has not transitioned to a novel state. Reef-matrix cores extracted from this reef reveal that the coral community has remained in this state for over 800 years, suggesting long-term stability and resistance to the region-wide shift to novel states. Without these data to provide historical context, this potentially robust and stable reef would be overlooked since it does not fulfil expectations of what a Caribbean coral reef should look like in the absence of humans. This example illustrates how defining past variation using the fossil record can improve our understanding of modern degradation and guide conservation.

Environmental change drove macroevolution in cupuladriid bryozoans.

Most macroevolutionary events are correlated with changes in the environment, but more rigorous evidence of cause and effect has been elusive. We compiled a 10 Myr record of origination and extinction, changes in mode of reproduction, morphologies and abundances of cupuladriid bryozoan species, spanning the time when primary productivity collapsed in the southwestern Caribbean as the Isthmus of Panama closed. The dominant mode of reproduction shifted dramatically from clonal to aclonal, due in part to a pulse of origination followed by extinction that was strongly selective in favour of aclonal species. Modern-day studies predict reduced clonality in increasingly oligotrophic conditions, thereby providing a mechanistic explanation supporting the hypothesis that the collapse in primary productivity was the cause of turnover. However, whereas originations were synchronous with changing environments, extinctions lagged 1-2 Myr. Extinct species failed to become more robust and reduce their rate of cloning when the new environmental conditions arose, and subsequently saw progressive reductions in abundance towards their delayed demise. Environmental change is therefore established as the root cause of macroevolutionary turnover despite the lag between origination and extinction.

Reconstructing reef fish communities using fish otoliths in coral reef sediments.

Little is known about long-term changes in coral reef fish communities. Here we present a new technique that leverages fish otoliths in reef sediments to reconstruct coral reef fish communities. We found over 5,400 otoliths in 169 modern and mid-Holocene bulk samples from Caribbean Panama and Dominican Republic mid-Holocene and modern reefs, demonstrating otoliths are abundant in reef sediments. With a specially-built reference collection, we were able to assign over 4,400 otoliths to one of 56 taxa (35 families) though mostly at genus and family level. Many otoliths were from juvenile fishes for which identification is challenging. Richness (by rarefaction) of otolith assemblages was slightly higher in modern than mid-Holocene reefs, but further analyses are required to elucidate the underlying causes. We compared the living fish communities, sampled using icthyocide, with the sediment otolith assemblages on four reefs finding the otolith assemblages faithfully capture the general composition of the living fish communities. Radiocarbon dating performed directly on the otoliths suggests that relatively little mixing of sediment layers particularly on actively accreting branching coral reefs. All otolith assemblages were strongly dominated by small, fast-turnover fish taxa and juvenile individuals, and our exploration on taxonomy, functional ecology and taphonomy lead us to the conclusion that intense predation is likely the most important process for otolith accumulation in reef sediments. We conclude that otolith assemblages in modern and fossil reef sediments can provide a powerful tool to explore ecological changes in reef fish communities over time and space.

Young species of cupuladriid bryozoans occupied new Caribbean habitats faster than old species.

The breadth of habitat occupied by a species, and the rate at which a species can expand into new habitats has important ecological and evolutionary consequences. Here we explore when extant species of free-living cupuladriid bryozoans expanded into new benthic Caribbean habitats that emerged during the final stages of formation of the Isthmus of Panama. Habitat breadth was estimated using the abundances of over 90,000 colonies in ten cupuladriid species, along with the ecological and sedimentary characteristics of the samples in which they occurred. Data reveal that all species expanded their habitat breadths during the last 6 Myr, but did so at a different tempo. 'Young' species - those that originated after 5 Ma - expanded relatively quickly, whereas 'old' species - those that originated before 9 Ma - took a further 2 Myr to achieve a comparable level of expansion. We propose that, like invasive species, young species are less restrained when expanding their habitat breadths compared to older well-established species. Understanding the mechanism causing this restraint requires further research.

Prehistorical and historical declines in Caribbean coral reef accretion rates driven by loss of parrotfish.

Caribbean coral reefs have transformed into algal-dominated habitats over recent decades, but the mechanisms of change are unresolved due to a lack of quantitative ecological data before large-scale human impacts. To understand the role of reduced herbivory in recent coral declines, we produce a high-resolution 3,000 year record of reef accretion rate and herbivore (parrotfish and urchin) abundance from the analysis of sediments and fish, coral and urchin subfossils within cores from Caribbean Panama. At each site, declines in accretion rates and parrotfish abundance were initiated in the prehistorical or historical period. Statistical tests of direct cause and effect relationships using convergent cross mapping reveal that accretion rates are driven by parrotfish abundance (but not vice versa) but are not affected by total urchin abundance. These results confirm the critical role of parrotfish in maintaining coral-dominated reef habitat and the urgent need for restoration of parrotfish populations to enable reef persistence.