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Biology subjects

Fifer, J. E.

Publications and source records attributed to Fifer, J. E..

9 recordsLinked to original sources

Rapid urban evolution of the dengue mosquito in West African cities

Aedes aegypti is an exceptionally effective global vector of human disease because of its strong specialization on human hosts and habitats. However, in its native range in Africa, many populations never specialized on humans and retained an ancestral generalist ecology. Now, in the rapidly growing cities of Kumasi, Ghana and Ouagadougou, Burkina Faso, we directly document genomic and behavioral evidence of a sudden shift towards greater specialization on humans over just five years. These changes are likely to enhance the ability of these urban mosquito populations to serve as effective vectors of human disease and may have played a role in unprecedented recent outbreaks of dengue fever in West African cities.

evolutionary biology↗

Ecological genomics of preference for human hosts in the native range of the dengue mosquito

The arbovirus transmitting mosquito Aedes aegypti has African origins where it maintains generalist and human specialist feeding forms, the latter of which has recently expanded their range worldwide. These two different forms appear to be directly linked to discrete genetic lineages, where the relative proportion of each ancestry dictates a mosquitos standing on the human specialist-generalist behavior spectrum. Here we take a population genomics approach to develop a predictive model for describing the distribution of human specialist behavior across Africa. We show genome-wide ancestry is predictive of human specialist behavior, but a subset of the genome offers even greater predictability. We also show that an ecological model incorporating precipitation, temperature and human density explains the geographic patterning of human specialist behavior in Africa.

evolutionary biology↗

Genomic signatures of coral adaptation and recovery following a mass mortality event

Globally, corals face an increased frequency of mass mortality events (MMEs) as populations experience repeated marine heatwaves which disrupt their obligate algal symbiosis. Despite greater occurrences of MMEs, the relative roles of the environment, host, and symbiont genetic variation in survival and recovery remain unresolved. We explore these roles using high-resolution temporal and spatial whole genome sequencing of corals before, after, and several years following a MME. We show that host genetics has an impact on bleaching and mortality and that selected alleles important for adaptation persist through the next generation. We also demonstrate that survival for the bleaching event was highly polygenic and that allele frequency shifts have reef habitat specificity. This study reveals how MMEs reshape the genomic landscape and the spatial and temporal distribution of genomic diversity within coral populations facing severe threats from global change. SIGNIFICANCEInvestigations of natural selection in coral genomes following bleaching events have primarily relied on indirect inference, using contemporary populations to explore signatures of past selective pressures, or failed to link these events to the subsequent generation. This has left an open question about the ability of a coral population to adapt from host standing genetic variation in the face of a bleaching event. We demonstrate rapid evolution in a Moorean coral population following an MME from a marine heatwave by capturing allele frequency shifts through time. However, the complex polygenic architecture of bleaching survival shows strong habitat specificity, complicating the path towards a genomic prediction of bleaching.

evolutionary biology↗

Outside your shell: how temperature shapes genetic variation in two species of congeneric marine snails

Intertidal organisms withstand extreme temperature fluctuations, and their ability to cope with this variation may affect their distributions across the seascape. Genetic variation and local environments likely interact to determine variation in thermal performance across intertidal species ranges, so characterizing the relationship between temperature variation and population structure is key to understanding the biology of marine invertebrates. Here, we use 2bRAD-sequencing to examine population genetic structure in two congeneric intertidal marine gastropods (Crepidula fornicata, C. plana), sampled from locations along a natural temperature gradient on the Northeast shores of the United States. These two species share similar life histories, yet C. plana exhibits a narrower distribution than C. fornicata. Our results demonstrate that both species show patterns of genetic divergence consistent with isolation by distance, though this pattern was only significant in C. fornicata. Both putatively selected and neutral loci displayed significant spatial structuring in C. fornicata; however, only putatively selected loci showed significant clustering in C. plana. When exploring whether temperature differences explained genetic differentiation, we found that 9-12% of genetic differentiation was explained by temperature variation in each species even when controlling for latitude and neutral population structure. Our results suggest that temperature shapes adaptive variation across the seascape in both Crepidula species and encourages further research to differentiate our results from models of neutral evolutionary drift.

evolutionary biology↗

Cryptic diversity shapes coral symbioses, physiology, and response to thermal challenge

Coral persistence in the Anthropocene is shaped by interactions among holobiont partners (coral animals, microbial symbionts) and their environment. Cryptic coral lineages-genetically distinct yet morphologically similar groups-are critically important as they often exhibit functional diversity relevant to thermal tolerance. Additionally, environmental parameters such as thermal variability may promote tolerance, but how variability interacts with holobiont partners to shape responses to thermal challenge remains unclear. Here, we identified three cryptic lineages of Siderastrea siderea in Bocas del Toro, Panama that differ in distributions across inshore and offshore reefs, microbial associations, holobiont phenomes, and skeleton morphologies. A thermal variability experiment failed to increase thermal tolerance, but subsequent thermal challenge and recovery revealed one lineage maintained elevated energetic reserves, photochemical efficiency, and growth. Lastly, coral cores highlighted that this lineage also exhibited faster growth historically. Functional variation among cryptic lineages highlights their importance in predicting coral reef responses to climate change. TeaserCryptic host diversity drives coral phenotypes relevant to climate change.

evolutionary biology↗

Distinct modes of holobiont specialization among cryptic coral lineages

As ocean warming threatens reefs worldwide, identifying corals with adaptations to higher temperatures is critical for conservation. Genetically distinct but morphologically similar (i.e., cryptic) coral populations can be specialized to extreme habitats and thrive under stressful conditions. These corals often associate with locally beneficial microbiota (Symbiodiniaceae photobionts and bacteria), clouding interpretation of the drivers of thermal tolerance. Here, we leverage a holobiont (massive Porites) with high host-partner fidelity to investigate adaptive variation across classic ("typical" conditions) and extreme reefs characterized by higher temperatures and light attenuation. We uncovered three cryptic lineages that exhibit limited micro-morphological variation; one lineage dominated classic reefs (L1), one had more even distributions (L2), and a third was restricted to extreme reefs (L3). Two lineages were more closely related to populations [~]4300 km away, suggesting that these lineages are widespread. All corals harbored Cladocopium C15 photobionts, but strain-level compositions differed among lineages and reef types. L1 associated with distinct photobionts and bacteria in each reef type, whereas L2 had relatively stable associations. L3 hosted unique photobiont strains, signaling high host-photobiont fidelity. Analysis of light harvesting capacity and thermal tolerance revealed key adaptive variation underpinning survival in distinct habitats. L1 had the highest light absorption efficiency and lowest thermal tolerance, suggesting it is a classic reef specialist. L3 had the lowest light absorption efficiency and the highest thermal tolerance, showing that it is an extreme reef specialist. L2 had intermediate light absorption efficiency and thermal tolerance, signaling habitat generalism, potentially explaining how it survives well in both habitat types. These findings reveal diverging holobiont strategies to cope with extreme conditions. Resolving coral lineages is key to understanding variation in thermal tolerance among coral populations; uncovering thermally-tolerant holobionts can strengthen our understanding of coral evolution and symbiosis, and support global conservation and restoration efforts.

ecology↗

Marine heatwaves threaten cryptic coral diversity and erode associations amongst coevolving partners

Climate change-amplified heatwaves are known to drive extensive mortality in marine foundation species. However, a paucity of longitudinal genomic datasets has impeded understanding of how these rapid selection events alter species genetic structure. Impacts of these events may be exacerbated in species with obligate symbioses, where the genetics of multiple co-evolving species may be affected. Here, we tracked the symbiotic associations and fate of reef-building corals for six years through a prolonged heatwave. Coral genetics strongly predicted survival of the common coral Porites through the event, with strong differential survival (15 to 64%) apparent across morphologically identical -but genetically distinct- lineages. The event also disrupted strong associations between coral lineages and their symbiotic partners, homogenizing symbiotic assemblages across lineages and reducing the specificity of coral-algal symbioses. These results highlight that marine heatwaves threaten cryptic genetic diversity of foundation species and have the potential to decouple tight relationships between co-evolving host-symbiont pairs.

ecology↗

Starvation Decreases Immunity and Immune Regulatory Factor NF-κB in the Starlet Sea Anemone Nematostella vectensis

Lack of proper nutrition (malnutrition) or the complete absence of all food (starvation) have important consequences on the physiology of all organisms. In many cases, nutritional status affects immunity, but, for the most part, the relationship between nutrition and immunity has been limited to studies in vertebrates and terrestrial invertebrates. Herein, we describe a positive correlation between nutrition and immunity in the sea anemone Nematostella vectensis. Gene expression profiling of adult fed and starved anemones showed downregulation of many genes involved in nutrient metabolism and cellular respiration, as well as immune-related genes, in starved animals. Starved adult anemones also had reduced protein levels and DNA-binding activity of immunity-related transcription factor NF-{kappa}B. Starved juvenile anemones had increased sensitivity to bacterial infection and also had lower NF-{kappa}B protein levels, as compared to fed controls. Weighted Gene Correlation Network Analysis (WGCNA) revealed significantly correlated gene networks that were inversely associated with starvation. Based on the WGCNA and a reporter gene assay, we identified TRAF3 as a likely NF-{kappa}B target gene in N. vectensis. Overall, these experiments demonstrate a correlation between nutrition and immunity in a basal marine metazoan, and the results have implications for the survival of marine organisms as they encounter changing environments. Significance StatementAdequate nutrition is required to sustain proper biological function. One factor threatening many marine organisms, as a result of modern day anthropogenic environmental changes, is nutrient availability. Here, we characterize transcriptional changes following food deprivation in the cnidarian model sea anemone Nematostella vectensis. We show that starvation is correlated with decreased expression of genes associated with nutrient metabolism and immunity, among others. Moreover, starvation reduces the level of expression and activity of immune regulatory transcription factor NF-{kappa}B and causes anemones to have increased susceptibility to bacterial infection. These results demonstrate that this basal organism responds at the transcriptional level to the absence of food, and that, in addition to changes in metabolic factors, starvation leads to a reduction in immunity.

immunology↗

Demographic Inferences and Loci Under Selection in a Recently Expanded Coral Population

Coral poleward range expansions in response to warming oceans have been historically observed, however contemporary expansion rates of some coral species have become more rapid as global temperatures rise at unprecedented rates. Range expansion can lead to reduced genetic diversity and surfing of deleterious mutations in expanding populations, potentially limiting the ability for adaption and persistence in novel environments. Successful expansions that overcome these founder effects and colonize new habitat have been attributed to multiple introductions from different sources, hybridization with native populations, or rapid adaptive evolution. Here, we investigate population genomic patterns of the reef-building coral Acropora hyacinthus along a latitudinal cline that includes a well-established range expansion front in Japan using 2b-RAD sequencing. A total of 184 coral samples were collected across seven sites spanning from [~]24{degrees}N to near its northern range front at [~]33{degrees}N. We uncover the presence of three cryptic lineages of A. hyacinthus, which occupy discrete areas within this region. Only one lineage is present at the expansion front and we find evidence of its historical occupation of marginal habitats. Within this lineage we also find evidence of bottleneck pressures associated with expansion events including higher clonality, increased linkage disequilibrium, and lower genetic diversity in range edge populations compared to core populations. Asymmetric migration between populations was also detected with lower migration from edge sites. Lastly, we describe genomic signatures of local adaptation potentially attributed to lower winter temperatures experienced at the more recently expanded northern populations. Together these data illuminate the genomic consequences of range expansion in a coral and highlight how adaptation to colder temperatures along the expansion front may facilitate further range expansion in this coral lineage.

evolutionary biology↗