Ph.D. - Zoology

Permanent URI for this collectionhttps://hdl.handle.net/10125/2173

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Salt-crossed lovers: A genomic investigation of adaptive potential in hybridizing saltwater and freshwater mesoamerican crocodiles (Crocodylus acutus and Crocodylus moreletii)
(University of Hawai'i at Manoa, 2025) Sung, Helen Winter; Reed, Floyd; Zoology
Hybridization presents both a conservation challenge and an evolutionary opportunity – particularly where natural hybrid zones intersect with human-modified landscapes. Recent advances in genomics have reshaped our understanding of hybridization, revealing its role in facilitating adaptation and diversification, especially in dynamic environments. In this dissertation, I investigate the evolutionary and conservation implications of naturally occurring hybridization between two Mesoamerican crocodile species in Belize: Crocodylus acutus (American crocodile) and Crocodylus moreletii (Morelet’s crocodile). Using reduced-representation genomic data, I first characterized population structure, admixture dynamics, and demographic history. These analyses revealed widespread admixture, the presence of two genetically distinct C. acutus lineages in Belize, and evidence of both ancient and ongoing hybridization. Building upon this foundation, I examined the genetic architecture of salinity tolerance – a key ecological trait delineating species boundaries. Through genome-wide association scans (GWAS), I identified two candidate loci associated with environmental salinity gradients, including a previously uncharacterized sodium channel gene (SCN5A-like) in archosaurs. These findings suggest that introgressed variants may contribute to physiological adaptation in hybrid populations. Finally, I assessed the role of adaptive introgression in shaping hybrid genomes. By integrating genome-wide scans for recent positive selection with tests of interspecific gene flow and window-based introgression analyses, I identified introgressed genomic regions under selection enriched in genes linked to environmental stress response, osmoregulation, and metabolism. Notably, introgression patterns were asymmetric, with directional gene flow shaping distinct genomic regions through historical versus recent admixture. Together, these findings suggest that hybridization in crocodylians is not merely a consequence of anthropogenic disturbance but may serve as a mechanism of evolutionary innovation. This work deepens our understanding of hybridization in long-lived vertebrates and underscores the importance of recognizing hybrids as valuable contributors to biodiversity. By integrating genomic and ecological perspectives, this dissertation aims to inform conservation strategies for species affected by hybridization, particularly those subject to uneven legal protections and complex evolutionary trajectories.
Molecules to management: Navigating uncertainty in environmental DNA biomonitoring of coral reefs
(University of Hawai'i at Manoa, 2025) Nichols, Patrick Kendall; Marko, Peter; Zoology
Environmental DNA (eDNA) tools are transforming biodiversity assessments, offering a powerful, minimally intrusive way to obtain comprehensive biological information from genetic traces in the environment. While the promise of guiding conservation decision-making across disciplines is immense, its reliability for routine monitoring remains uncertain, constrained by biological complexity and methodological limitations that influence detection dynamics. This dissertation evaluated the performance of eDNA tools across layered sources of uncertainty, from ecological variability to methodological biases, to assess their effectiveness for coral reef monitoring. First, eDNA surveys were evaluated for their ability to capture temporal variation at multiple reef sites in Hawai‘i and to identify the seasonal drivers that lead to community-wide shifts in biodiversity. Next, the impact of different eDNA collection methods on the detection of cryptic reef taxa that are otherwise difficult to survey was assessed. Finally, the sensitivity of eDNA for detecting rare species was tested by validating a novel assay for the nuisance macroalga Chondria tumulosa. To interpret inherently uncertain molecular detections, site-occupancy detection models calibrated with visual survey data were used. These models quantify false positives and false negatives, and estimate key parameters for integrating eDNA into applied conservation and management decisions. By addressing spatial, ecological, and technical sources of variability, this work offers an assessment of eDNA reliability and its readiness for integration into real-world coral reef monitoring efforts, including long-term ecological assessments, early detection of invasive species, and tracking biodiversity responses to management interventions. While the transformative potential of eDNA is clear, successful implementation depends on rigorous testing, strategic trade-offs, and transparent accounting for uncertainty.
Insights into ‘opihi and ‘ōpelu fisheries using oceanographic modeling, experiments, and sociological investigations
(University of Hawai'i at Manoa, 2025) Mukai, Gabriella Nobuko Mazaira; Moran, Amy L.; Zoology
Distribution and abundance of marine resources are affected by various abiotic and biotic factors ranging from temperature, dissolved oxygen, presence or absence of competitors, and food availability. In this dissertation, I examined the role of several environmental variables in shaping distribution and abundance of two important living resources in Hawai‘i, ‘Opihi Makaiauli (Limpet, Cellana exarata) and ‘Ōpelu (Mackerel Scad, Decapterus macarellus), through larval development experiments and larval transport models (‘Opihi), and fisher interviews and species distribution models (‘Ōpelu). ‘Opihi Makaiauli is one of three endemic limpet species in Hawai‘i, collectively referred to as ‘Opihi. For ‘Opihi Makaiauli, larval development and time to metamorphosis have been reported in the literature only once and how water temperature affects the ability of embryos and larvae to develop and survive has not yet been determined for any of the three species, to our knowledge. The two studies that have modeled larval dispersal of ‘Opihi Makaiauli included several islands in the Hawaiian chain, but connectivity has not been modeled across the entire archipelago. In my first data chapter (Chapter 2), I evaluated the effects of temperature on the survival of embryos and larvae of ‘Opihi Makaiauli and described the timing of their development from fertilization to metamorphic competence. I applied the result from the larval rearing experiment to my second data chapter (Chapter 3), a larval transport model of ‘Opihi Makaiauli. For my third data chapter (Chapter 4), I evaluated the environmental factors influencing ‘Ōpelu aggregation behavior and catchability by combining fisher knowledge and fishery-dependent data to create a model of ‘Ōpelu catch.
Chromosome number evolution and the diversification of ray-finned fishes
(University of Hawai'i at Manoa, 2025) Worsham, McLean; Porter, Megan; Zenil-Ferguson, Rosana; Zoology
Ray-finned fishes account for nearly half of all vertebrate species today and are arguably the most phenotypically diverse vertebrate clade in Earth’s history. Across this great species richness, they also exhibit many axes of trait diversity. One trait which varies widely is haploid chromosome number, ranging from 6 to 223, although most species have 23–25 chromosomes. Prior research has found that evolution of chromosome number can affect gene expression, meiosis, and gametic compatibility—mechanisms that may influence speciation. Therefore, this study is focused on the macroevolutionary impacts that chromosome number evolution may have on the evolution and diversification of Actinopterygii (ray-finned fishes). First, I tested three hypotheses to explain why an observed central tendency of ~24 haploid chromosomes is so prevalent across distantly related lineages. My findings emphasize that descending dysploidy—loss of individual chromosomes—is a fast and important mechanism in fish chromosome evolution. This process, which may be a component of rediploidization, contributes to the retention of ~24 chromosomes even in lineages that have undergone polyploidy. Descending dysploidy may also be advantageous by reducing the energetic cost of cell division, helping maintain genomic stability. My results further show that chromosome number evolution is a dynamic process shaped by both biotic and abiotic factors. Traits such as dispersal ability, climatic niche, salinity, water depth, fertilization mode, and parental care all interact in complex ways to influence chromosomal change, making it challenging to disentangle their individual effects. Finally, I examined how chromosome number evolution relates to speciation and diversification. Using state-dependent diversification models, I found that the cumulative number of polyploidy events—rather than polyploidy itself—modulates diversification rates. In some cases, polyploidy appears to accelerate diversification and in others, it slows it, offering a potential explanation for the conflicting conclusions of earlier studies which have long debated the impact of whole genome duplications on speciation and diversification. Still, these patterns raise fundamental evolutionary questions such as: if polyploidy can enhance diversification, why don’t we see species with infinite chromosome numbers? Furthermore, if descending dysploidy is such a prevalent process why stop at 24 chromosomes instead of reducing all the way down to one? My results suggest that the explanation may not be reduceable to a single dimension (i.e., chromosome number), but rather diversification outcomes depend on unobserved (i.e., not yet measured) traits, which modulate how lineages respond to chromosomal changes. Identifying these “hidden” factors could be key to understanding how genomic architecture and standing genetic variation shape evolutionary potential across macroevolutionary time and the actinopterygian tree of life.
Larval and thermal ecology of Antarctic marine invertebrates: It's pretty cool
(University of Hawai'i at Manoa, 2025) Toh, Ming Wei Aaron; Moran, Amy L.; Zoology
The Southern Ocean surrounding Antarctica is one of the coldest and most thermally stable marine environments on the planet and hosts a diverse and highly endemic array of life. Cold-blooded organisms that have evolved in these waters share traits such as high temperature sensitivity, slow pace of growth and development, large eggs, and prevalence of brooding. Little is known about the reproductive ecology of one of its inhabitants, the Antarctic pycnogonid, or sea spider. We investigated patterns of organic mass loss during early development in two species of brooding sea spiders (Ammothea glacialis and Nymphon australe) and found that development is largely fueled by yolk reserves, though later larval stages in N. australe may supplement nutrition through exogenous feeding while brooded. Due to climate change, the Antarctic has become one of the fastest-warming regions on Earth, and the stenothermal organisms that inhabit the Southern Ocean are now faced with developmental and physiological challenges caused by rising temperatures. We examined the effects of small increases in temperature (-1.8, -0.4, +1 and +4 °C) on survival, energetic content, and developmental timing of the embryos and larvae of the same two species of sea spider as above, and two additional species of nudibranch (Tritoniella belli and Tritonia challengeriana). We found that, while sea spiders exhibited minimal mortality across treatments, nudibranch survival declined sharply at higher temperatures. Energetic content of embryos and larvae was generally lower with warming, attributed to lower protein reserves, and developmental length was shortened at higher temperatures. The estimated cost of development was lowest at 0.4 °C or +1 °C for most species, suggesting that current ambient temperatures (-1.8 °C) may be suboptimal for energetic efficiency of embryonic or larval development, and that future warming beyond +1°C could lead to metamorphosis with lower energetic reserves. Climate change is also predicted to increase both the frequency and intensity of marine heatwaves in the Southern Ocean, where a severe event in 2022 saw temperature fluctuations of nearly 2°C in a single week. We tested the ability of adult Antarctic snails (Neobuccinum eatoni) to acclimate to short-term warming, using noninvasive infrared heart rate sensors. Following a two-week exposure to 4°C, snails exhibited increased cardiac performance at warmer temperatures, demonstrating physiological plasticity on a shorter timescale than previously recorded in other Antarctic taxa. Together, these findings suggest that Antarctic marine invertebrates may exhibit resilience to moderate warming up to +1°C, but higher temperatures could reduce energetic efficiency of early development, with potential implications for juvenile survival and ecosystem stability under future climate scenarios.
Effects of temperature on the embryonic cleavage rates and larval metabolism of Antarctic invertebrates
(University of Hawai'i at Manoa, 2025) Lobert, Graham Thomas; Moran, Amy; Zoology
Global climate change is set to disrupt global ecosystems with changes to both biotic and abioticenvironmental factors. The world’s oceans are warming at unprecedented rates, with temperature increases of between +1.4 °C and +4.4 °C expected by 2100. These increases in temperature particularly threaten the biota and ecosystems in the high Antarctic regions of Southern Ocean where temperatures have been cold (~ -1.8 °C) and thermally stable for over 30 million years. Warming temperatures can disrupt the biochemical reactions and physiological processes within an individual organism, with potential follow-on effects on populations and ecosystems. The organisms that inhabit the Southern Ocean are adapted to life within a very cold and narrow temperature range and are believed to have limited ability to cope with temperature stress. In this dissertation, I examine how temperature impacts early embryonic cleavage and metabolism, processes that are common to all metazoans. Our study subjects were four species of benthic Antarctic ectotherms, two pycnogonids (Nymphon australe and Ammothea glacialis), and two dendronotid nudibranchs (Tritoniella belli and Tritonia challengeriana). I first investigated the effects of temperature on the early cleavage phase. I found that for all four species, embryonic cleavage rate increased rapidly as temperature increased from -1.8 °C (ambient) to +3.5 °C. Consistent with other rate processes that have been measured in Antarctic marine ectotherms, the thermal sensitivity of cleavage rate was high. We also found that overall, thermal sensitivity was very high within the species’ natural temperature range (-1.8 to ~0 C), but cleavage rate was less affected by temperature increases above the natural temperature range. This suggests that organisms haven’t fully adapted to polar conditions potentially due to the limits of protein synthesis in extremely cold temperatures. Second, I investigated the effects of temperature on the metabolic rate (as estimated from oxygen consumption) of early, middle, and late larval stages from the same four species. I found that the thermal sensitivity of oxygen consumption was high for the majority of stages, with 8/12 exhibiting Q10 values higher than the 2-4 generally seen for most biological functions. Specific stages of development did not seem to affect thermal sensitivity. Lastly, I investigated the ability of larvae of one of the four species (Nymphon australe) to acclimate to temperature. In most Antarctic ectotherms tested to date, acclimation was completely absent or slow, requiring months to acclimate. I found that after 24 days at +1.0 °C, III larvae N. australe had lower overall oxygen consumption rates than those of larvae incubated at - 1.8 °C for the same period, a classic sign of thermal acclimation. This is the first time that acclimation has been shown in Antarctic invertebrate larvae. Signs of acclimation occurred in weeks as opposed to months shown by adults of Antarctic invertebrates. Larvae of N. australe may be able to optimize their metabolism to match environmental temperature fluctuations and predicted warming on an ecologically relevant time scale. Together, this work shows that the two essential processes of early cleavage and larval metabolism are thermally sensitive to small increases in temperature. However, if particularly sensitive stages, such as early larval stages, can acclimate to warming waters as shown here, Antarctic ectotherms may be more robust to warming than previously thought.
INVESTIGATING MICROBIOME ASSEMBLY AND ITS IMPACT ON THE PHYSIOLOGY OF AEDES ALBOPICTUS (DIPTERA: CULICIDAE)
(University of Hawai'i at Manoa, 2024) Griffin, Chasen; Medeiros, Matthew C.I.; Zoology
Mosquito-borne disease is a major public health burden globally despite decades of efforts towards its eradication. Mosquitoes are difficult to control and many of the most important vectors of human pathogens have developed resistance to conventional insecticides—highlighting the urgency to find novel ways to control mosquito-borne diseases. In recent years, the mosquito microbiome has been the subject of intense study and has revealed interesting insights into its role in mosquito biology. The microbiome is highly influential in shaping many biological processes of mosquitoes including development, fecundity, immunity, metabolism, and nutrient acquisition. Much of a host’s microbiome is derived from the environment; thus, the composition of the environmental microbiome is an important driver of host microbiome composition, which could lead to phenotypic heterogeneity between mosquito populations on the landscape—further complicating control efforts. In Hawaiʻi, the non-native and highly invasive mosquito, Aedes albopictus, is well established, but microbiome-driven phenotypic heterogeneity in populations is not well understood. Therefore, I developed three projects to explore how exposure to compositionally manipulated environmental microbiomes impact A. albopictus biological and physiological processes. The first project involved the reintroduction of environmental bacteria to an A. albopictus colony that was originally isolated from Mānoa, Oʻahu, Hawaiʻi and had been in the laboratory for 15 generations. To vary the environmental microbial community composition, a series of filters were implemented to manipulate the community by cell size that included: a 10 μm regimen, a 2 μm regimen, a 0.1 μm regimen, and a Millipore filter. Mesocosms were created from the filtrates and A. albopictus were reared as larvae into adulthood. Using generalized linear mixed models (GLMM), microbiome α- and β-diversity of the adults from each mesocosm was investigated. The mesocosm microbiomes were also compared to wild A. albopictus pupae that were collected in the environmental water and to wild A. albopictus adults collected near the habitats. The results showed that α-diversity did not differ between the filtered mesocosms; however, the microbiomes of mesocosms were significantly different from wild pupae and from wild adults. The β-diversity analysis showed that the microbiomes of the 10 μm and 2 μm mesocosms formed a single group, the 0.1 μm and Millipore mesocosms formed a single group, wild pupae formed a single group, and wild adults formed a single group. Development times were also measured. Pupation occurred 1.59 days earlier in the 10 μm and the 2 μm mesocosms compared to the 0.1 μm and Millipore mesocosms. The ability of adults to survive under starvation was also impacted by the mesocosm from which they emerged. Adults from the 0.1 μm and Millipore mesocosms survived approximately twice as long as those from the 10 μm and 2 μm mesocosms. These findings demonstrate that exposure to compositionally distinct environmental microbiomes impact i) the assembly of the host microbiome and ii) important biological processes within the host in different ways. In the second project, a more comprehensive exploration of the A. albopictus microbiome was performed. Mosquitoes collected from Makiki, Oʻahu, Hawaiʻi and their microbiomes were sequenced using the bacterial 16S rRNA gene and the microbial fungal internal transcribed spacer (ITS) gene. Three networks were generated: a 16S only network, an ITS only network, and a cross-domain network. To test the stability of the networks, attacks on the networks were targeted at the centrality measures of node degree (a measure of how many connections one node makes to another node) and betweenness (the total number of shortest paths from node to node). The cross-domain network showed the highest stability in the face of attacks, remaining more stable as more nodes removed from the network. A keystone species analysis was also performed using the same centrality measures and of the six highest taxa fungi comprised five of those, further indicating the importance of fungi in the A. albopictus microbiome. Using the hypothesis that fungi were influential in the stability of the microbiome, a similar experiment to project one was conducted but added a 30-50 μm filter that allowed for environmental fungi to pass into the filtrate. β-diversity was assessed using GLMMs and the presence of fungi in the filtrate led to different microbial communities structures than when fungi are not present. Those results are interesting not only because they validate and support the theoretical network models that generated the hypothesis but emphasize the necessity of including fungi in A. albopictus microbiome studies. The third project investigated the impacts of developing in compositionally distinct microbial habitats on critical physiological processes in A. albopictus. Those processes were development time, development success, fatty acid synthesis, the ability to survive under starvation, and immune function. All physiological processes were impacted by exposure to compositionally distinct environmental microbiomes and varied by filtration level. Furthermore, the ability to withstand starvation and immune expression, both measured in adult mosquitoes, was impacted by the sex of the mosquitoes and also varied by filtration level. Overall, this study highlights the importance of exposure to compositionally distinct environmental microbiomes on A. albopictus physiology. Furthermore, these findings emphasize the need to include fungi, which are often omitted, in A. albopictus microbiome experiments because of their importance in structuring the microbiome.
Source to sink: Modeling marine population connectivity across scales in the Main Hawaiian Islands
(University of Hawai'i at Manoa, 2024) Conklin, Emily Elizabeth; Toonen, Robert; Zoology
Coral reef ecosystems are some of the most diverse ecosystems on the planet, and are culturally, economically, and ecologically valuable. In Hawaiʻi, coral reefs provide a host of ecosystem goods and services, including but not limited to commercial and subsistence fishing, coastal protection, and recreation. These reefs provide an estimated >7 million meals per year, and have been valued at $33.57 billion based on ecosystem services. Given the importance of Hawaiʻi reef-associated fisheries for subsistence, cultural continuity, and food security, effective management of these ecosystems is essential in the face of ongoing environmental decline due to both local and global stressors. Connectivity is a crucial component of the long-term functioning of a network of marine managed areas, but is seldom included in spatial planning despite its inclusion in global conservation goals. In this dissertation, I combined biophysical larval dispersal modeling with network analysis to describe potential connectivity patterns across scales. The goals of my dissertation were to model and describe fine-scale patterns of connectivity around the island of Molokaʻi, with particular focus on the role of protected areas (Chapter 2), expand the model to the entire Main Hawaiian Islands, examine the effects of behavior on larval dispersal, and compare model output to population genomics data (Chapter 3), and use network analysis of the historic Indigenous management regime (the moku system) to highlight key potential connectivity hubs (Chapter 4). Species-specific patterns of connectivity were present in both the Molokaʻi and Main Hawaiian Islands models; dispersal distance was correlated with pelagic larval duration, but rank-order did not match exactly. I also found that active-behavior models differed significantly from passive models for this region, and that active-behavior models outperformed passive models when compared to multispecies population genomic data. Finally, I used network metrics to estimate source-sink dynamics for both the Molokaʻi and Main Hawaiian Islands models, identifying potential diverse source sites and multigenerational stepping-stones. These results provide stakeholders and managers with crucial information for current and future marine spatial planning in the region and highlight opportunities for future research.
THE PHYSIOLOGY AND MOLECULAR ECOLOGY OF VISION IN HAWAIIAN SEABIRDS
(University of Hawai'i at Manoa, 2024) Moon, Hannah E.; Porter, Megan; Zoology
Spectral sensitivity is considered highly similar among bird species, despite well documented differences in the spectral sensitivities of other vertebrate species (i.e. fish) based on ecology and light environment. Seabirds function across complex light environments; displaying diurnal, crepuscular, and nocturnal activity, foraging in open ocean water to various depths, forming nesting colonies anywhere from barren rocky cliffs to burrowing in dense forests, all while simultaneously coping with the visual transition between air and water - all factors known to shape vision. Because studies of vision in birds primarily focus on land birds, seabirds are understudied yet an ideal group to test the assumption that vision is similar among birds. In this dissertation I challenge the prevailing idea that avian vision is similar among species through the physiological characterization of vision in Hawaiian seabirds and propose a novel molecular framework for the modulation of color vision across all avian species. The aims of this work are threefold: 1) Quantify physiological differences in spectral and temporal response to light using electroretinograms from adult and juvenile birds in three target species of endangered and locally threatened birds in Hawai’i (Pterodroma sandwichensis, Puffinus newelli, and Ardenna pacifica); 2) Using retinal transcriptomes from A. pacifica, identify a novel molecular mechanism in bird eyes capable of rapidly modulating light response; 3) Explore expression patterns and ecological correlations of this novel molecular mechanism using retinal transcriptomes from 17 species of Hawaiian sea- and waterbirds. Here, I present physiological evidence of species-specific variation in spectral, temporal, and absolute sensitivity in vision between three closely related seabird species. Additionally, I present molecular evidence of novel alternative splicing of visual proteins and describe the functionality of alternative splicing as a method for rapid adaptation of vision in birds. Finally, I identify the widespread use of alternative splicing of visual proteins in avian species and propose potential applications of alternative splicing in avian vision beyond the species in this dissertation. Unanswered questions about the specific drivers and functionality of alternative splicing of visual proteins lay the groundwork for a novel field of research and an abundance of opportunities for future studies of avian vision and visual ecology.
RESILIENCE ACROSS GENERATIONS: EXPLORING TRANSGENERATIONAL AND LARVAL ACCLIMATION TO THERMAL STRESS IN THE MARINE ANNELID HYDROIDES ELEGANS
(University of Hawai'i at Manoa, 2024) Genovese, Caitlyn; Moran, Amy; Zoology
Temperature can have profound impacts on the reproductive and developmental aspects of marine ectotherms. I examined how varying temperatures impact egg size, energy content, larval survival, and settlement dynamics across generations in the marine annelid Hydroides elegans. This work aimed to highlight the adaptive mechanisms marine invertebrates may employ to cope with rapidly changing oceanic temperatures. Through a series of interconnected studies, I explored the phenotypic plasticity of egg characteristics, thermal tolerance of larvae, settlement, and oxygen consumption rates, focusing on the significance of transgenerational and within-generation thermal responses. My first study investigated the effects of maternal rearing temperature on egg size, fecundity, and energy content in the marine annelid Hydroides elegans, a free-spawning benthic annelid invasive to Hawai'i. Results demonstrated that parental rearing temperature significantly affects egg size and fecundity, with cooler temperatures favoring larger eggs and higher fecundity. Interestingly, while egg size typically decreased with increasing temperature, the energy content of the eggs exhibited an inverse relationship, with smaller eggs from warmer temperatures containing more energy as well as higher energy densities This finding challenges the common assumption that larger eggs contain more energy, suggesting that temperature-driven changes in egg size may not align with adaptive responses but rather represent physiological constraints. My second study explored the thermal tolerance and survival strategies in larval stages of the marine annelid Hydroides elegans under varying thermal conditions. We investigated the roles of larval acclimation and maternal effects at different rearing temperatures to understand potential adaptive responses to thermal stress. We found significant effects of larval rearing temperature on thermal tolerance, with higher rearing temperatures generally corresponding to lower LT50 values, suggesting decreased thermal tolerance in larvae that were raised at the highest temperature. Maternal rearing temperature and the interaction between larval and maternal temperatures showed less consistent impacts on larval survival, inconsistent with the hypothesis that transgenerational plasticity significantly enhances thermal tolerance in this species. My final study investigated the influence of transgenerational and larval environmental temperatures on the settlement dynamics and metabolic rates of Hydroides elegans larvae. Conducted across a temperature gradient of 21°C, 25°C, and 29°C, this study examines whether parental exposure to elevated temperatures affects settlement rates and oxygen consumption (proxy for metabolic rate) of offspring. Results indicate day post fertilization was the only factor affecting settlement rate but that larval rearing temperature significantly affects metabolic rates, with larvae at 29°C displaying higher oxygen consumption, suggesting an increase in energy expenditure per unit time. Conversely, parental temperature showed only a marginal influence on larval settlement, with no significant transgenerational effects on metabolic rates.
It's all about the journey: insights into invasion history from the lizards of the Hawaiian Islands
(University of Hawai'i at Manoa, 2024) Alvarez, Valentina; Thomson, Robert C.; Zoology
The rapid population growth and subsequent range expansion of humans over the last several millennia has led to numerous introductions of organisms outside their native ranges. This has occurred repeatedly in Hawaiʻi, which now houses a large and growing collection of introduced plants and animals. This includes at least thirty species of terrestrial reptile that have been established over the last centuries, seven of which are thought to have arrived on voyaging canoes. The introduction of reptiles to Hawaiʻi at multiple time points in history offers an opportunity to investigate how the pattern and timing of biological introductions might be inferred using information contained in the genomes of introduced populations. I reconstructed the invasion histories of three species of lizard introduced to Hawaiʻi at different points in time. The first species, the brown anole (Anolis sagrei), is well known for its ability to invade new regions and rapidly outcompete native species. In Hawaiʻi, this species appeared in the 1980s and prior genetic work suggests a Florida origin. More recently, the brown anole has become established in Southern California and anecdotal evidence suggest Hawaiʻi may be the source of some of these introductions. The second species, the house gecko (Hemidactylus frenatus), is native to southeast Asia but is now established across the Pacific. With its first collection in Hawaiʻi in 1947, it is thought to have been introduced via increased maritime activity associated with World War II. Lastly, the Oceania snake-eyed skink (Cryptoblepharus poecilopleurus) is considered a canoe species and was first collected in Hawaiʻi in 1840. However, recent phylogenetic work has suggested that populations in Hawaiʻi are distinct from others in the Pacific. This, paired with their known ability to disperse long distances and widespread presence across the Pacific, presents the possibility of a natural dispersal of this species to the Hawaiian Islands. We pair likelihood-based and approximate methods such as approximate Bayesian computation (ABC) to study the invasion histories of these species. By reconstructing these histories, we aim to provide insight into potential pathways of species introduction and colonization for each species, while testing hypotheses about the context and timing of each invasion.
ECOLOGY OF FISHES AND INVERTEBRATES INHABITING THE CORAL POCILLOPORA GRANDIS IN HAWAIʻI
(University of Hawai'i at Manoa, 2024) Brush, Erik Grosvenor; Hixon, Mark; Zoology
The environmental variables and biological interactions that shape biological communities have long been a major focus of the science of ecology. When much of the physical structure of the community is biogenic, such as on coral reefs, these factors affect the living habitat itself. Coral reefs around most of Hawaiʻi are characterized by large seasonal waves, low coral cover, and low coral species richness. The antler coral, Pocillopora grandis, an uncommon member of the coral community, can grow to more than 1.5 meters in diameter. At this size, these highly branching colonies attract substantial assemblages of resident fishes and invertebrates in an otherwise low-lying reefscape that lacks other substantial sources of vertical relief. Antler coral may therefore provide disproportionately important habitat space relative to its total abundance. Surveys at three sites across the southern shore of Oʻahu revealed that reefscape-scale factors had little effect on resident assemblage structure. Most variation in fish and invertebrate assemblages was attributed to colony volume and amount of living tissue, yet there was evidence of agonistic interactions between species, especially at smaller colony sizes. Given these behavioral observations, I conducted a six-month experimental removal of two common residents, the Blue-eye Damselfish (an interference competitor) and the Arc-eye Hawkfish (a mesopredator). Resident fish and invertebrate abundance and species richness were significantly greater in the absence of these strong interactors. Finally, using photogrammetry, I measured host colony growth rates during this experiment on both manipulated and unmanipulated colonies. In the absence of Blue-eye Damselfish, predation on host colonies by coral-eating fishes greatly increased, resulting in reduced growth rates and sometimes mortality. This pattern provided evidence for a novel indirect mutualism on coral reefs in which a territorial corallivore indirectly benefits its host coral through defense against transient corallivores, reducing total corallivory and increasing host colony growth. Furthermore, on unmanipulated coral colonies, resident fish identity likely affected the magnitude of augmented growth acquired by the host, with species spending more time in direct contact with the colony providing a greater benefit. Despite limited colonization by other fishes when Blue-eye Damselfish and Arc-eye Hawkfish were already present, these two species provided multiple benefits that increased growth and survival of host P. grandis colonies.
Competition And Resource Partitioning Between Congeneric Coral- Dwelling Scorpionfishes (sebastapistes Spp.) In Hawai‘i
(University of Hawaii at Manoa, 2023) Jones, Ryan Neil; Hixon, Mark A.; Zoology
Exposed coral reefs in Hawai‘i are largely dominated by the small branching cauliflower coral (Pocillopora meandrina), which supports diverse communities of fishes and invertebrates. Two of the most common fishes that reside in these corals are the Speckled Scorpionfish (Sebastapistes coniorta) and the Galactic Scorpionfish (S. galactacma). These small nocturnal reef mesopredators use the complex branching morphology of cauliflower coral as protection during the day and feed in and around their host corals at night. Despite their apparent ecological similarities, these species coexist locally, at times even co-occupying the same host coral. Surveys of cauliflower coral communities around O‘ahu revealed inverse depth distributions, with Galactic Scorpionfish found across all depths surveyed, though more commonly in deeper reef areas (> 11 m), while Speckled Scorpionfish almost exclusively occurred in shallow reef areas (5 – 10 m deep). These species also used microhabitat in subtly different ways, with the larger species (Speckled Scorpionfish) being more associated with coral colonies with wider spacing between branches. Reciprocal removal experiments across depths, among clusters of corals, and within individual colonies suggest that competition between these species is not currently occurring, and recolonization experiments showed that colony characteristics played a large role in determining which species recolonized corals. Diet analyses using both visual examination and DNA metabarcoding of stomach contents revealed that Speckled Scorpionfish and Galactic Scorpionfish have minimally overlapping diets with significantly different compositions, though both species typically consume small crustaceans that co-occur with them in cauliflower corals. Further, the diets of these species did not significantly differ whether they co-occurred or not, suggesting that these species have evolved different diets, possibly due to past competition. Thus, these species partition food and microhabitat resources to a degree that presently allows for their coexistence on reefs in Hawai‘i.
Impact Of Environment, Host Microbiome, And Stress On Angiostrongylus Cantonensis (rat Lungworm) Transmission
(University of Hawaii at Manoa, 2023) Rollins, Randi; Cowie, Robert; Zoology
Angiostrongylus cantonensis, commonly known as rat lungworm, is a nematode parasite widely distributed in tropical and subtropical regions, and is the causative agent of neuroangiostrongyliasis, a leading cause of eosinophilic meningitis globally. This parasite completes its life-cycle in various gastropod species (intermediate host) and rat species (definitive host). Humans are accidental hosts, becoming infected by ingesting infectious stage larvae, present in snails. Symptoms of neuroangiostrongyliasis can be severe, occasionally leading to death. Other mammals and birds also serve as accidental hosts. Although A. cantonensis was originally discovered in 1935, it wasn’t linked to human disease until 1961, when found in the brain of a deceased Hawaiʻi State Hospital patient. Since 1961, the parasite’s life-cycle and distribution have been discovered, but relatively little is known about A. cantonensis. Therefore, I developed three projects to explore the effects of the environment, stress, and host microbial communities on host-parasite dynamics and human transmission. The first project involved the collection of 16 snail species from 39 sites across Oʻahu, where A. cantonensis infection prevalence and intensity were determined using qPCR targeting the ITS1 region of DNA. Generalized linear mixed models (GLMMs) were constructed, incorporating environmental data to assess the influence of rainfall and temperature on these infection metrics. The analysis revealed higher infection prevalence and intensity in snails inhabiting wetter, cooler regions compared to snails in hotter, drier areas. In the second project, 196 snails (Parmarion martensi) were subjected to stress, leading to the release of infectious larvae in 13.3% of the stressed snails’ slime, while non-stressed snails did not release any larvae. Permutation tests and GLMMs demonstrated that stress significantly alters the parasite-host relationship, with snail infection intensity positively correlated with the presence of A. cantonensis larvae in their slime. These findings suggest that snail slime may serve as an alternative zoonotic transmission pathway. The third project involved a comparison of the effect of A. cantonensis infection on the microbial communities of snail guts (Parmarion martensi and Lissachatina fulica), rat feces and rat skin (Rattus rattus and R. norvegicus) using high-throughput sequencing of 16S ribosomal RNA. Analysis of microbial abundance with GLMMs revealed a significant interaction between infection status, host species, and individual bacteria. Shifts in individual bacterial abundances in response to A. cantonensis infection were most pronounced in the gut microbiota of infected snails, characterized by large log2FoldChange values. Changes in microbial abundance in rat feces were less pronounced, and relatively minor in rat skin. Notably, certain bacterial groups displayed remarkable increases in abundance in both taxa, suggesting potential protective symbiosis in response to A. cantonensis infection. Furthermore, differences in host susceptibility were observed to be associated with varying degrees of microbial disturbance. Parmarion martensi, a highly susceptible snail host, exhibited less microbial dysbiosis than L. fulica, a less susceptible host, suggesting the existence of unique adaptations and coadaptations in host-parasite interactions, potentially driven by the evolutionary history of the parasite and host. These projects contribute to the understanding of host-parasite relationships and provide valuable ecological insights for future research on A. cantonensis. The findings highlight the risk for human neuroangiostrongyliasis in different environments, the influence of stress in disease transmission, and the potential for microbial targets to be developed for therapeutic intervention and disease prevention. Furthermore, these discoveries have implications for ongoing efforts to mitigate human transmission and disease caused by A. cantonensis.
Vision and Bioluminescence of Marine Crustaceans
(University of Hawaii at Manoa, 2023) Iwanicki, Tom; Porter, Megan L.; Zoology
The overarching theme of this dissertation research was to understand light as the cue for life in the ocean. I approached this dissertation with a background in molecular biology, animal behavior, and vertebrate opsin evolution, and upon my arrival was tasked with familiarizing myself with invertebrate opsins and bioluminescence. Chapter 1 briefly describes my rationale for this dissertation research and puts it into a broader context for understanding light as a cue for light in the ocean. Chapter 2 contains a literature review of the many multiple origins, forms and functions, cellular biology, and ecology of bioluminescence, with an emphasis on marine taxa. I point to recent discoveries in bioluminescent systems that challenge orthodoxies and present a systematic review of plausible human impacts on bioluminescence via ocean acidification. In chapter 3, I present a fully resolved molecular phylogeny for metridinid copepods, with an emphasis on the genus Pleuromamma, and characterize the opsin and luciferase diversity in the group using transcriptomics. Within the transcriptomes, I found evidence for the origin of copepod bioluminescence possibly arising from a blood clotting protein. In chapter 4, I used immunohistochemistry to localize opsin proteins in ocular and non-ocular tissues from four species in the superfamily Oplophoroidea, a group of bioluminescent decapod shrimp. These data provide molecular confirmation for previously described single- and dual-sensitivity visual systems in the superfamily, and offer the first evidence for co-localization of opsins in the R8 cells – or distal rhabdom – of a decapod crustacean retina. In chapter 5, I sequenced metatranscriptomes from zooplankton communities at Station ALOHA, Oʻahu, Hawaiʻi to describe community structure across the epipelagic and lower mesopelagic during the day and night for small and large zooplankton. We found that Station ALOHA was dominated by copepods, followed by euphausiids, amphipods, and ostracods, with a faunal shift toward fishes in large bodied, deep samples, and time of day had no influence on overall community structure. Further, we tested the utility of metatranscriptomes for functional analysis leveraging gene expression estimates of the opsin gene family. We found that opsin abundance does not conform with community patterns and that depth, size, and taxa influenced opsin expression, but time of day had no effect. Combined, these chapters leverage tools at multiple levels of organization to understand why bioluminescence is such a prevalent phenomenon throughout the worlds oceans, and to understand how visual ecology structures where species are horizontally, temporally, and vertically through the water column.
The Power Of Poop: Insights Into Hawaiian Honeycreeper Conservation Through DNA Metabarcoding
(University of Hawaii at Manoa, 2022) Costantini, Maria Sara; Reed, Floyd A.; Zoology
The Hawaiian honeycreeper lineage (subfamily: Carduelinae) is one of the quintessential examples of an adaptive radiation. In modern human history, however, most of the 56+ species that evolved from a Eurasian finch have gone extinct, and most of the extant species are experiencing severe population declines. Currently, urgent management actions are being taken to prevent the extinction of the lineage, including captive breeding and translocation efforts. In this dissertation, I used DNA metabarcoding of fecal samples to study the diets and gut microbiomes (GM) of Hawaiian honeycreepers and inform management decisions of these imperiled species. I first focused on two critically endangered species that have recently been brought into captivity for conservation breeding efforts. Previous work on other species have shown that captivity can negatively affect individuals’ gut microbiome. The GM is known to strongly influence the health, fitness, and behavior of its hosts, yet what drives its formation and how the GM is affected by environmental changes is not well understood across species. I then characterized the diet of the forest birds on the island of Kauaʻi, which has been an island of particular concern due to the recent rapid population declines of several species. I found that Lepidoptera are key components of all bird diets regardless of foraging guild, that there is evidence for resource partitioning between closely related species, and that the diet of an introduced bird is not distinct from native species. Finally, I investigated how three main factors contribute to the composition of GMs across the extant Hawaiian honeycreeper lineage. I looked at the relative roles of host phylogeny, diet, and geography, and found that geographic distance was associated with the largest effect on the variation within honeycreeper microbiomes. The results from this dissertation work can be used by wildlife managers to improve Hawaiian honeycreeper conservation strategies, protecting and bolstering the populations of these stunning species into the future.
Patterns and Processes Shaping Avian Diversity in the Hawaiian Islands
(University of Hawaii at Manoa, 2022) Campillo, Luke; Thomson, Robert C.; Zoology
Species are fundamental units of biology. However, the way we define the boundaries between species is a topic of much debate. The process of defining species limits, also known as species delimitation, has historically relied heavily on one factor: reproductive isolation. The importance of reproductive isolation in the history of speciation research is hard to overstate. Most contemporary evolutionary biologist, however, accept that reproductive isolation is not the only thing that matters for species delimitation. Moreover, recognizing that species boundaries are not neatly defined, along with technological and computational advancements, has driven a conceptual shift in our understanding of the formation and maintenance of species boundaries. Researchers are now able to probe the patterns and processes driving speciation in new ways. Among the most important paradigm shifts has been a broad implementation of the Multispecies Coalescent (MSC) framework. Under the MSC conceptual framework we are no longer limited by the strict requirement of reproductive isolation (or any other single factor), but instead aim to understand the genetic history of individuals within populations. In my dissertation, I use MSC-based methods to investigate species delimitation patterns and the speciation processes across different levels of evolutionary divergence and taxonomic breadth. In the first dissertation chapter, I used data from over a century of mating trials in Drosophia flies and contemporary DNA sequence data to determine if species delimited based on reproductive isolation are the same as those identified using a MSC method. In the second dissertation chapter, I obtained DNA sequence data from thousands of genetic markers to and sophisticated phylogenetic methods to determine the evolutionary history for an endemic group of birds known collectively as ‘Elepaio. For the third chapter, I obtained whole genome sequence data from a single species from the Hawaiian honeycreeper radiation, ‘Apapane, to investigate how genomic differentiation may influence the early stages of the speciation process.
Advances In Monitoring, Assessing, And Predicting Condition Of The Coral Holobiont
(University of Hawaii at Manoa, 2022) Greene, Austin L.; Donahue, Megan J.; Zoology
Rising incidence of coral disease is one of the most pressing contemporary impacts occurring on modern coral reefs, leading to local extinctions of coral genera and challenging coral conservation efforts on a global scale. Differing physiology of coral species and complex microbial ecologies combine with diverse anthropogenic impacts to make prediction of coral disease or its mediation difficult. These challenges are compounded by a lack of affordable methods to monitor visual coral health or detect latent impacts before visual signs of coral disease become apparent. I address these topics across the six central chapters of this thesis. In Chapter 2, I develop an affordable field-ready camera system to persistently monitor coral reef environments and reduce barriers for under-resourced managers to track visual coral health. In Chapter 3, I develop a step-by-step guide designed to encourage molecular analysis of corals as a holobiont, wherein I walk users through sampling designs, sample collection, and sample preservation for later use in analysis of the coral microbiome, metabolome, and histology. Demonstrating the value of collecting longitudinal datasets, in Chapter 4 I analyze 72,000 coral colony observations collected over a period of nine years and identify drivers of coral White Syndrome diseases that are consistent across coral species in Guam. I follow this study in Chapter 5 with an intensive investigation of a White Syndrome outbreak affecting Pocillopora damicornis in Guam, using methods developed in Chapter 2 to describe early molecular signatures of this disease and a potential mechanism of disease resilience in this coral species. In the last sections of this dissertation, I assess the future of coral reefs by investigating the effects of coral diversity on the microbiome and the latent impacts affecting near-shore coral communities. In Chapter 6, I establish through a manipulative experiment that the microbiome of Pocillopora acuta is unaffected by changes to coral diversity, but growth of this species frequently used in restoration efforts is significantly determined by the surrounding coral community. Lastly, in Chapter 7, I use untargeted coral metabolomics to study the dominant Hawaiian coral Montipora capitata and establish that coral communities on Maui are bioaccumulating of contaminants tied to local land use with unknown effects on coral health. Collectively, these diverse chapters demonstrate that coral conservation is ripe for technological innovation as well as the use of molecular methods in reef management, leading to new insights into the health and resilience of coral reefs.
Stepping Out Of The Shadows: Genomic And Experimental Illumination Of Diversity Within The Coral Family Agariciidae
(University of Hawaii at Manoa, 2022) Lewis, Claire Jennifer; Marko, Peter B.; Zoology
Confidently delimiting species and resolving their evolutionary histories relies on accurate taxonomy and well-supported phylogenies; two things which have been historically challenging in corals. The coral family Agariciidae is composed of species with exceptionally large ranges, and therefore likely contains numerous cryptic species. The aims of this dissertation are to study the phenotypic variation, phylogenomic and geographic diversity of species from the family Agariciidae. To assess the phylogenetics and phylogeography of this family I applied two approaches. First, I used a traditional mitochondrial DNA barcoding approach that focused effort on a taxonomically and geographically broad sampling scheme. I combined 208 new sequences with 191 previously published sequences, representing 31 species. Relationships based on the mtDNA intron revealed considerable discordance between the current taxonomy and recovered clades; just seven species were recovered as monophyletic. Second, I generated RAD libraries for a subset of individuals, which produced far more data from across the genome, albeit from fewer samples (120), which represented twenty nominal taxa. From these libraries I assembled complete mitochondrial genomes, 18 of which are the first recorded for that taxon. I estimated phylogenies from SNPs generated from three different assembly approaches. Both the mitogenome and SNP phylogenies recovered well-supported trees, but they were not fully concordant with one another. I found no evidence of introgression within the SNP datasets, indicating hybridization may not be as prevalent in this family as in some other corals. The SNP trees recovered three well-supported clades, none of which corresponded to a monophyletic Pavona or Leptoseris. Each phylogenetic data set recovered multiple putative cryptic species associated with the nominal taxa P. varians and L. mycetoseroides. Both species form similar encrusting, ridged colonies, indicating this morphology may be the ancestral state of this family or may have evolved independently multiple times. Given the evolutionary and ecological success of the ridged morphology, combined with the high variability both within and between species, I examined the extent of light-associated phenotypic plasticity for P. varians. A common garden experiment revealed light had a strong effect on both the growth rates and morphology of colonies. This is likely an adaptive response which allows this depth generalist species to tolerate a wide variety of light environments. Overall this work suggests whole genome studies and further experiments are necessary to fully resolve the species boundaries and evolutionary processes driving speciation in this family.
Insights From An Introduced Lizard On Coping With Environmental Change: Is It Better To Be Behaviorally Flexible Or Consistent?
(University of Hawaii at Manoa, 2022) Screen, Robyn; Wright, Amber N.; Zoology
Brown anoles (Anolis sagrei) are native to Cuba and the Bahamas, but have been widely introduced to other Caribbean islands, the southeastern United States, Hawai‘i, and Japan. While some traits have been used to model their ability to become naturalized in new locations (Latella et al. 2011) behavior has been largely unexplored. Some studies have begun to test their learning ability (Storks and Leal 2020) and their behavioral consistency (called behavioral syndromes) (Lapiedra et. al. 2016) but both studies are limited by either low sample size or studying only one sex. I used non-native populations of brown anoles on the island of Oʻahu in the Hawaiian Islands, USA to test for the presence of a boldness syndrome and to test their learning ability. Behavioral syndromes are theorized to be favored in environments where one consistent behavior maximizes fitness. This could play an important role in responding to novel challenges and opportunities in urban habitats. Previous research indicates that urban individuals tend to be more aggressive, exploratory, and bold than their rural conspecifics (Sih et al. 2004a). I measured a behavioral syndrome along the bold-shy axis across eight populations along an urban gradient and compared boldness among sites, but boldness was not significantly different when comparing my urban and rural sites. A syndrome was detected, but was weak in strength, indicating low within-individual consistency in boldness. Behavioral flexibility via the ability to learn is another way for non-native animals to cope with new environments. Learning ability has mostly been studied in mammals and birds, but studies on reptiles are becoming more prevalent (e.g., Szabo et al. 2018, Storks and Leal 2020, De Meester et al. 2021). I measured problem-solving ability and learning-ability in 66 wild-caught lizards. I presented lizards with a detour task, a clear plastic tube with one entrance, over subsequent trials and measured their time to complete the task in each trial. About half of the lizards showed the ability to problem-solve by completing the task at least once. Only 9 of the 66 lizards decreased their solve-time over trials, indicating the ability to learn. I next evaluated the field of behavioral syndromes through a literature review and simulations. I found that, despite earlier recommendations to increase sample sizes (Garamszegi et al. 2012), many studies in this field are still underpowered. Simulations revealed that underlying mixtures of syndrome strength within a population can be obscured by correlation and mixed model analyses. I demonstrate and recommend the use of maximum pairwise differences to quantify these underlying patterns.

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