Two Tickets to Paradise: Multiple Dispersal Events in the Founding of Hoary Bat Populations in Hawai'i

The Hawaiian islands are an extremely isolated oceanic archipelago, and their fauna has long served as models of dispersal in island biogeography. While molecular data have recently been applied to investigate the timing and origin of dispersal events for several animal groups including birds, insects, and snails, these questions have been largely unaddressed in Hawai''i’s only native terrestrial mammal, the Hawaiian hoary bat, Lasiurus cinereus semotus. Here, we use molecular data to test the hypotheses that (1) Hawaiian L. c. semotus originated via dispersal from North American populations of L. c. cinereus rather than from South American L. c. villosissimus, and (2) modern Hawaiian populations were founded from a single dispersal event. Contrary to the latter hypothesis, our mitochondrial data support a biogeographic history of multiple, relatively recent dispersals of hoary bats from North America to the Hawaiian islands. Coalescent demographic analyses of multilocus data suggest that modern populations of Hawaiian hoary bats were founded no more than 10 kya. Our finding of multiple evolutionarily significant units in Hawai''i highlights information that should be useful for re-evaluation of the conservation status of hoary bats in Hawai''i.     

Invasion of the Hawaiian Islands by a parasite infecting imperiled stream fishes

Points of origin and pathways of spread are often poorly understood for introduced parasites that drive disease emergence in imperiled native species. Co‐introduction of parasites with non‐native hosts is of particular concern in remote areas like the Hawaiian Islands, where the introduced nematode Camallanus cotti has become the most prevalent parasite of at‐risk native stream fishes. In this study, we evaluated the prevailing hypothesis that C. cotti entered the Hawaiian Islands with poeciliid fishes from the Americas, and spread by translocation of poeciliid hosts across the archipelago for mosquito control. We also considered the alternative hypothesis of multiple independent co‐introductions with host fishes originating from Asia. We inferred conduits of introduction and spread of C. cotti across the archipelago from geographic patterns of mtDNA sequence variation and allelic variation across 11 newly developed microsatellite markers. The distribution of haplotypes suggests that C. cotti spread across the archipelago following an initial introduction on O'ahu. Approximate Bayesian Computation modeling and allelic variation also indicate that O'ahu is the most likely location of introduction, from which C. cotti dispersed to Maui followed by spread to the other islands in the archipelago. Evidence of significant genetic structure across islands indicates that contemporary dispersal is limited. Our findings parallel historical records of non‐native poeciliid introductions and suggest that remediating invasion hotspots could reduce the risk of infection in native stream fishes, which illustrates how inferences on parasite co‐introductions can improve conservation efforts by guiding responses to emerging infectious disease in species of concern.     

Incipient radiation within the dominant Hawaiian tree Metrosideros polymorpha

Although trees comprise a primary component of terrestrial species richness, the drivers and temporal scale of divergence in trees remain poorly understood. We examined the landscape-dominant tree, Metrosideros polymorpha, for variation at nine microsatellite loci across 23 populations on young Hawai''i Island, sampling each of the island''s five varieties throughout its full geographic range. For four varieties, principal coordinate analysis revealed strong clustering of populations by variety across the 10 430 km² island, indicating partitioning of the species into multiple evolutionarily significant units. The single island-endemic form, riparian var. newellii, showed especially strong differentiation from other varieties despite occurring in sympatry with other varieties and likely evolved from a bog form on the oldest volcano, Kohala, within the past 500 000 years. Along with comparable riparian forms on other Pacific Islands, var. newellii appears to represent parallel incipient ecological speciation within Metrosideros. Greater genetic distance among the more common varieties on the oldest volcano and an inverse relationship between allelic diversity and substrate age appear consistent with colonization of Hawai''i Island by older, partially diverged varieties followed by increased hybridization among varieties on younger volcanoes. This study demonstrates that broad population-level sampling is required to uncover patterns of diversification within a ubiquitous and long-lived tree species. Hawaiian Metrosideros appears to be a case of incipient radiation in trees and thus should be useful for studies of divergence and the evolution of reproductive isolating barriers at the early stages of speciation.     

Why are marine adaptive radiations rare in Hawai'i?

Islands can be sites of dynamic evolutionary radiations, and the Hawaiian Islands have certainly given us a bounty of insights into the processes and mechanisms of diversification. Adaptive radiations in silverswords and honeycreepers have inspired a generation of biologists with evidence of rapid diversification that resulted in exceptional levels of ecological and morphological diversity. In this issue of Molecular Ecology, tiny waterfall‐climbing gobies make a case for their place among Hawaiian evolutionary elite. Moody et al. ( 2015 ) present an analysis of gene flow and local adaptation in six goby populations on Kaua'i and Hawai'i measured in three consecutive years to try to disentangle the relative role of local adaptation and gene flow in shaping diversity within Sicyopterus stimpsoni. Their study shows that strong patterns of local selection result in streams with gobies adapted to local conditions in spite of high rates of gene flow between stream populations and no evidence for significant genetic population structure. These results help us understand how local adaptation and gene flow are balanced in gobies, but these fishes also offer themselves as a model that illustrates why adaptive diversification in Hawai'i's marine fauna is so different from the terrestrial fauna.     

Large‐scale introduction of the Indo‐Pacific damselfish Abudefduf vaigiensis into Hawai'i promotes genetic swamping of the endemic congener A. abdominalis

Hybridization in the ocean was once considered rare, a process prohibited by the rapid evolution of intrinsic reproductive barriers in a high‐dispersal medium. However, recent genetic surveys have prompted a reappraisal of marine hybridization as an important demographic and evolutionary process. The Hawaiian Archipelago offers an unusual case history in this arena, due to the recent arrival of the widely distributed Indo‐Pacific sergeant (Abudefduf vaigiensis), which is hybridizing with the endemic congener, A. abdominalis. Surveys of mtDNA and three nuclear loci across Hawai'i (N = 396, Abudefduf abdominalis and N = 314, A. vaigiensis) reveal that hybridization is significantly higher in the human‐perturbed southeast archipelago (19.8%), tapering off to 5.9% in the pristine northwest archipelago. While densities of the two species varied throughout Hawai'i, hybridization was highest in regions with similar species densities, contradicting the generalization that the rarity of one species promotes interspecific mating. Our finding of later generation hybrids throughout the archipelago invokes the possibility of genetic swamping of the endemic species. Exaptation, an adaptation with unintended consequences, may explain these findings: the endemic species has transient yellow coloration during reproduction, whereas the introduced species has yellow coloration continuously as adults, in effect a permanent signal of reproductive receptivity. Haplotype diversity is higher in Hawaiian A. vaigiensis than in our samples from the native range, indicating large‐scale colonization almost certainly facilitated by the historically recent surge of marine debris. In this chain of events, marine debris promotes colonization, exaptation promotes hybridization, and introgression invokes the possible collapse of an endemic species.     

Vertical and Horizontal Genetic Connectivity in Chromis verater,an Endemic Damselfish Found on Shallow and Mesophotic Reefs in the Hawaiian Archipelago and Adjacent Johnston Atoll

Understanding vertical and horizontal connectivity is a major priority in research on mesophotic coral ecosystems (30–150 m). However, horizontal connectivity has been the focus of few studies, and data on vertical connectivity are limited to sessile benthic mesophotic organisms. Here we present patterns of vertical and horizontal connectivity in the Hawaiian Islands-Johnston Atoll endemic threespot damselfish, Chromis verater, based on 319 shallow specimens and 153 deep specimens. The mtDNA markers cytochrome b and control region were sequenced to analyze genetic structure: 1) between shallow (<30 m) and mesophotic (30–150 m) populations and 2) across the species'' geographic range. Additionally, the nuclear markers rhodopsin and internal transcribed spacer 2 of ribosomal DNA were sequenced to assess connectivity between shallow and mesophotic populations. There was no significant genetic differentiation by depth, indicating high levels of vertical connectivity between shallow and deep aggregates of C. verater. Consequently, shallow and deep samples were combined by location for analyses of horizontal connectivity. We detected low but significant population structure across the Hawaiian Archipelago (overall cytochrome b: Φ_ST = 0.009, P = 0.020; control region: Φ_ST = 0.012, P = 0.009) and a larger break between the archipelago and Johnston Atoll (cytochrome b: Φ_ST = 0.068, P<0.001; control region: Φ_ST = 0.116, P<0.001). The population structure within the archipelago was driven by samples from the island of Hawaii at the southeast end of the chain and Lisianski in the middle of the archipelago. The lack of vertical genetic structure supports the refugia hypothesis that deep reefs may constitute a population reservoir for species depleted in shallow reef habitats. These findings represent the first connectivity study on a mobile organism that spans shallow and mesophotic depths and provide a reference point for future connectivity studies on mesophotic fishes.     

Incipient ecological speciation between successional varieties of a dominant tree involves intrinsic postzygotic isolating barriers

Whereas disruptive selection imposed by heterogeneous environments can lead to the evolution of extrinsic isolating barriers between diverging populations, the evolution of intrinsic postzygotic barriers through divergent selection is less certain. Long‐lived species such as trees may be especially slow to evolve intrinsic isolating barriers. We examined postpollination reproductive isolating barriers below the species boundary, in an ephemeral hybrid zone between two successional varieties of the landscape‐dominant Hawaiian tree, Metrosideros polymorpha, on volcanically active Hawai'i Island. These archipelago‐wide sympatric varieties show the weakest neutral genetic divergence of any taxon pair on Hawai'i Island but significant morphological and ecological differentiation consistent with adaptation to new and old lava flows. Cross‐fertility between varieties was high and included heterosis of F₁ hybrids at the seed germination stage, consistent with a substantial genetic load apparent within varieties through low self‐fertility and a lack of self‐pollen discrimination. However, a partial, but significant, barrier was observed in the form of reduced female and male fertility of hybrids, especially backcross hybrids, consistent with the accumulation of genetic incompatibilities between varieties. These results suggest that partial intrinsic postzygotic barriers can arise through disruptive selection acting on large, hybridizing populations of a long‐lived species.     

Skin resistance to water gain and loss has changed in cane toads (Rhinella marina) during their Australian invasion

The water‐permeable skin of amphibians renders them highly sensitive to climatic conditions, and interspecific correlations between environmental moisture levels and rates of water exchange across the skin suggest that natural selection adapts hydroregulatory mechanisms to local challenges. How quickly can such mechanisms shift when a species encounters novel moisture regimes? Cutaneous resistance to water loss and gain in wild‐caught cane toads (Rhinella marina) from Brazil, USA (Hawai''i) and Australia exhibited strong geographic variation. Cutaneous resistance was low in native‐range (Brazilian) toads and in Hawai''ian populations (where toads were introduced in 1932) but significantly higher in toads from eastern Australia (where toads were introduced in 1935). Toads from recently invaded areas in western Australia exhibited cutaneous resistance to water loss similar to the native‐range populations, possibly because toads are restricted to moist sites within this highly arid landscape. Rates of rehydration exhibited significant but less extreme geographic variation, being higher in the native range than in invaded regions. Thus, in less than a century, cane toads invading areas that impose different climatic challenges have diverged in the capacity for hydroregulation.     

Spread of an introduced parasite across the Hawaiian archipelago independent of its introduced host

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Dynamic Functional Modulation of CD4+ T Cell Recall Responses Is Dependent on the Inflammatory Environment of the Secondary Stimulus

The parameters that modulate the functional capacity of secondary Th1 effector cells are poorly understood. In this study, we employ a serial adoptive transfer model system to show that the functional differentiation and secondary memory potential of secondary CD4⁺ effector T cells are dependent on the inflammatory environment of the secondary challenge. Adoptive transfer of TCR transgenic lymphocytic choriomeningitis virus (LCMV) Glycoprotein-specific SMARTA memory cells into LCMV-immune hosts, followed by secondary challenge with Listeria monocytogenes recombinantly expressing a portion of the LCMV Glycoprotein (Lm-gp61), resulted in the rapid emergence of SMARTA secondary effector cells with heightened functional avidity (as measured by their ability to make IFNγ in response to ex vivo restimulation with decreasing concentrations of peptide), limited contraction after pathogen clearance and stable maintenance secondary memory T cell populations. In contrast, transfer of SMARTA memory cells into naïve hosts prior to secondary Lm-gp61 challenge, which resulted in a more extended infectious period, resulted in poor functional avidity, increased death during the contraction phase and poor maintenance of secondary memory T cell populations. The modulation of functional avidity during the secondary Th1 response was independent of differences in antigen load or persistence. Instead, the inflammatory environment strongly influenced the function of the secondary Th1 response, as inhibition of IL-12 or IFN-I activity respectively reduced or increased the functional avidity of secondary SMARTA effector cells following rechallenge in a naïve secondary hosts. Our findings demonstrate that secondary effector T cells exhibit inflammation-dependent differences in functional avidity and memory potential, and have direct bearing on the design of strategies aimed at boosting memory T cell responses.     

Knocking on Heaven's Door: Are Novel Invaders Necessarily Facing Na?ve Native Species on Islands?

The impact of alien predator species on insular native biota has often been attributed to island prey naïveté (i.e. lack of, or inefficient, anti-predator behavior). Only rarely, however, has the concept of island prey naïveté been tested, and then only a posteriori (i.e. hundreds or thousands of years after alien species introduction). The presence of native or anciently introduced predators or competitors may be crucial for the recognition and development of adaptive behavior toward unknown predators or competitors of the same archetype (i.e. a set of species that occupy a similar ecological niche and show similar morphological and behavioral traits when interacting with other species). Here, we tested whether two squamates endemic to New Caledonia, a skink, Caledoniscincus austrocaledonicus, and a gecko, Bavayia septuiclavis, recognized and responded to the odor of two major invaders introduced into the Pacific islands, but not yet into New Caledonia. We chose one predator, the small Indian mongoose Herpestes javanicus and one competitor, the cane toad Rhinella marina, which belong respectively to the same archetype as the following two species already introduced into New Caledonia in the nineteenth century: the feral cat Felis catus and the golden bell frog Litoria aurea. Our experiment reveals that geckos are naïve with respect to the odors of both an unknown predator and an unknown competitor, as well as to the odors of a predator and a competitor they have lived with for centuries. In contrast, skinks seem to have lost some naïveté regarding the odor of a predator they have lived with for centuries and seem “predisposed” to avoid the odor of an unknown potential competitor. These results indicate that insular species living in contact with invasive alien species for centuries may be, although not systematically, predisposed toward developing adaptive behavior with respect to species belonging to the same archetype and introduced into their native range.     

A Virulent Babesia bovis Strain Failed to Infect White-Tailed Deer (Odocoileus virginianus)

Wildlife are an important component in the vector-host-pathogen triangle of livestock diseases, as they maintain biological vectors that transmit pathogens and can serve as reservoirs for such infectious pathogens. Babesia bovis is a tick-borne pathogen, vectored by cattle fever ticks, Rhipicephalus spp., that can cause up to 90% mortality in naive adult cattle. While cattle are the primary host for cattle fever ticks, wild and exotic ungulates, including white-tailed deer (WTD), are known to be viable alternative hosts. The presence of cattle fever tick populations resistant to acaricides raises concerns regarding the possibility of these alternative hosts introducing tick-borne babesial parasites into areas free of infection. Understanding the B. bovis reservoir competence of these alternative hosts is critical to mitigating the risk of introduction. In this study, we tested the hypothesis that WTD are susceptible to infection with a B. bovis strain lethal to cattle. Two groups of deer were inoculated intravenously with either B. bovis blood stabilate or a larval extract supernatant containing sporozoites from infected R. microplus larvae. The collective data demonstrated that WTD are neither a transient host nor reservoir of B. bovis. This conclusion is supported by the failure of B. bovis to establish an infection in deer regardless of inoculum. Although specific antibody was detected for a short period in the WTD, the PCR results were consistently negative at multiple time points throughout the experiment and blood from WTD that had been exposed to parasite, transferred into naïve recipient susceptible calves, failed to establish infection. In contrast, naïve steers inoculated intravenously with either B. bovis blood stabilate or the larval extract supernatant containing sporozoites rapidly succumbed to disease. These findings provide evidence that WTD are not an epidemiological component in the maintenance of B. bovis infectivity to livestock.     

Antibody Profiling in Na?ve and Semi-immune Individuals Experimentally Challenged with Plasmodium vivax Sporozoites

BackgroundAcquisition of malaria immunity in low transmission areas usually occurs after relatively few exposures to the parasite. A recent Plasmodium vivax experimental challenge trial in malaria naïve and semi-immune volunteers from Colombia showed that all naïve individuals developed malaria symptoms, whereas semi-immune subjects were asymptomatic or displayed attenuated symptoms. Sera from these individuals were analyzed by protein microarray to identify antibodies associated with clinical protection.ConclusionClinical protection against experimental challenge in volunteers with previous P. vivax exposure was associated with elevated pre-existing antibodies, an attenuated serological response to the challenge and reactivity to new antigens.     

Will a warmer and wetter future cause extinction of native Hawaiian forest birds?

Isolation of the Hawaiian archipelago produced a highly endemic and unique avifauna. Avian malaria (Plasmodium relictum), an introduced mosquito‐borne pathogen, is a primary cause of extinctions and declines of these endemic honeycreepers. Our research assesses how global climate change will affect future malaria risk and native bird populations. We used an epidemiological model to evaluate future bird–mosquito–malaria dynamics in response to alternative climate projections from the Coupled Model Intercomparison Project. Climate changes during the second half of the century accelerate malaria transmission and cause a dramatic decline in bird abundance. Different temperature and precipitation patterns produce divergent trajectories where native birds persist with low malaria infection under a warmer and dryer projection (RCP4.5), but suffer high malaria infection and severe reductions under hot and dry (RCP8.5) or warm and wet (A1B) futures. We conclude that future global climate change will cause significant decreases in the abundance and diversity of remaining Hawaiian bird communities. Because these effects appear unlikely before mid‐century, natural resource managers have time to implement conservation strategies to protect this unique avifauna from further decimation. Similar climatic drivers for avian and human malaria suggest that mitigation strategies for Hawai'i have broad application to human health.     

Managing Conservation Reliant Species: Hawai'i's Endangered Endemic Waterbirds

Hawai''I''s coastal plain wetlands are inhabited by five endangered endemic waterbird species. These include the Hawaiian Coot (''alae ke''oke''o), Hawaiian Duck (koloa maoli), Hawaiian Stilt (ae''o), Hawaiian Gallinule (Moorhen) (''alae ''ula), and Hawaiian Goose (nēnē). All five species are categorized as being “conservation reliant.” The current strategy to recover these endangered birds includes land protection and active management of wetlands. To assess the effectiveness of the current management paradigm, we compared species population trends across the state to those on six actively managed wetland national wildlife refuges (Refuges) thought to be critical for the survival of these endangered species. To perform the evaluation we relied on systematic semiannual population counts that have been conducted across most wetlands in the state and monthly population counts that have occurred on Refuges during the same time period. We found that statewide and Refuge populations of the Hawaiian Coot, Stilt and Gallinule have rebounded from historic lows and over the last 20 years have slowly increased or remained stable. We also documented that Refuges are important to each species year-round and that a disproportionately larger percentage of the population for each species is found on them. Understanding of why Refuges successfully house a disproportionate percentage of these “conservation reliant” species can inform current and future conservation efforts as well as ensure long-term population viability for these species.     

In vivo CD8+ T Cell Dynamics in the Liver of Plasmodium yoelii Immunized and Infected Mice

Plasmodium falciparum malaria remains one of the most serious health problems globally and a protective malaria vaccine is desperately needed. Vaccination with attenuated parasites elicits multiple cellular effector mechanisms that lead to Plasmodium liver stage elimination. While granule-mediated cytotoxicity requires contact between CD8+ effector T cells and infected hepatocytes, cytokine secretion should allow parasite killing over longer distances. To better understand the mechanism of parasite elimination in vivo, we monitored the dynamics of CD8+ T cells in the livers of naïve, immunized and sporozoite-infected mice by intravital microscopy. We found that immunization of BALB/c mice with attenuated P. yoelii 17XNL sporozoites significantly increases the velocity of CD8+ T cells patrolling the hepatic microvasculature from 2.69±0.34 μm/min in naïve mice to 5.74±0.66 μm/min, 9.26±0.92 μm/min, and 7.11±0.73 μm/min in mice immunized with irradiated, early genetically attenuated (Pyuis4-deficient), and late genetically attenuated (Pyfabb/f-deficient) parasites, respectively. Sporozoite infection of immunized mice revealed a 97% and 63% reduction in liver stage density and volume, respectively, compared to naïve controls. To examine cellular mechanisms of immunity in situ, naïve mice were passively immunized with hepatic or splenic CD8+ T cells. Unexpectedly, adoptive transfer rendered the motile CD8+ T cells from immunized mice immotile in the liver of P. yoelii infected mice. Similarly, when mice were simultaneously inoculated with viable sporozoites and CD8+ T cells, velocities 18 h later were also significantly reduced to 0.68±0.10 μm/min, 1.53±0.22 μm/min, and 1.06±0.26 μm/min for CD8+ T cells from mice immunized with irradiated wild type sporozoites, Pyfabb/f-deficient parasites, and P. yoelii CS_280–288 peptide, respectively. Because immobilized CD8+ T cells are unable to make contact with infected hepatocytes, soluble mediators could potentially play a key role in parasite elimination under these experimental conditions.     

A Complex Evolutionary History in a Remote Archipelago: Phylogeography and Morphometrics of the Hawaiian Endemic Ligia Isopods

Compared to the striking diversification and levels of endemism observed in many terrestrial groups within the Hawaiian Archipelago, marine invertebrates exhibit remarkably lower rates of endemism and diversification. Supralittoral invertebrates restricted to specific coastal patchy habitats, however, have the potential for high levels of allopatric diversification. This is the case of Ligia isopods endemic to the Hawaiian Archipelago, which most likely arose from a rocky supralittoral ancestor that colonized the archipelago via rafting, and diversified into rocky supralittoral and inland lineages. A previous study on populations of this isopod from Oʻahu and Kauaʻi revealed high levels of allopatric differentiation, and suggested inter-island historical dispersal events have been rare. To gain a better understanding on the diversity and evolution of this group, we expanded prior phylogeographic work by incorporating populations from unsampled main Hawaiian Islands (Maui, Molokaʻi, Lanaʻi, and Hawaiʻi), increasing the number of gene markers (four mitochondrial and two nuclear genes), and conducting Maximum likelihood and Bayesian phylogenetic analyses. Our study revealed new lineages and expanded the distribution range of several lineages. The phylogeographic patterns of Ligia in the study area are complex, with Hawaiʻi, Oʻahu, and the Maui-Nui islands sharing major lineages, implying multiple inter-island historical dispersal events. In contrast, the oldest and most geographically distant of the major islands (Kauaʻi) shares no lineages with the other islands. Our results did not support the monophyly of all the supralittoral lineages (currently grouped into L. hawaiensis), or the monophyly of the terrestrial lineages (currently grouped into L. perkinsi), implying more than one evolutionary transition between coastal and inland forms. Geometric-morphometric analyses of three supralittoral clades revealed significant body shape differences among them. A taxonomic revision of Hawaiian Ligia is warranted. Our results are relevant for the protection of biodiversity found in an environment subject to high pressure from disturbances.     

Seasonal surveillance confirms the range expansion of Aedes japonicus japonicus (Theobald) (Diptera: Culicidae) to the Hawaiian Islands of Oahu and Kauai

The Asian bush mosquito, Aedes japonicus japonicus (Theobald) was not known to occur in the Hawaii archipelago until it was identified on the island of Hawaii in 2003. This mosquito species remained undetected on the neighboring islands for 8?years before it was discovered at the Honolulu International Airport on Oahu in 2012. By 2015, four Ae. j. japonicus mosquitoes were collected in the western mountains of Oahu and one was collected in the central mountains of Kauai. The collection of this invasive mosquito species across the neighboring Hawaiian Islands of Oahu and Kauai indicated the need for increased seasonal surveillance on these islands. Following nearly four years of surveillance, Ae. j. japonicus was also confirmed to occur in the eastern mountains of Oahu and in the central mountainous region of Kauai. To expand the knowledge of the spread of invasive mosquitoes species further surveillance is necessary to identify all possible areas where populations of Ae. j. japonicus and other invasive mosquito species occur in Hawaiian archipelago.