The diversity of influenza A viruses (IAV) is primarily hosted by two highly divergent avian orders: Anseriformes (ducks, swans and geese) and Charadriiformes (gulls, terns and shorebirds). Studies of IAV have historically focused on Anseriformes, specifically dabbling ducks, overlooking the diversity of hosts in nature, including gull and goose species that have successfully adapted to human habitats. This study sought to address this imbalance by characterizing spillover dynamics and global transmission patterns of IAV over 10 years at greater taxonomic resolution than previously considered. Furthermore, the circulation of viral subtypes in birds that are either host-adapted (low pathogenic H13, H16) or host-generalist (highly pathogenic avian influenza—HPAI H5) provided a unique opportunity to test and extend models of viral evolution. Using Bayesian phylodynamic modelling we uncovered a complex transmission network that relied on ecologically divergent bird hosts. The generalist subtype, HPAI H5 was driven largely by wild geese and swans that acted as a source for wild ducks, gulls, land birds, and domestic geese. Gulls were responsible for moving HPAI H5 more rapidly than any other host, a finding that may reflect their long-distance, pelagic movements and their immuno-naïve status against this subtype. Wild ducks, long viewed as primary hosts for spillover, occupied an optimal space for viral transmission, contributing to geographic expansion and rapid dispersal of HPAI H5. Evidence of inter-hemispheric dispersal via both the Pacific and Atlantic Rims was detected, supporting surveillance at high latitudes along continental margins to achieve early detection. Both neutral (geographic expansion) and non-neutral (antigenic selection) evolutionary processes were found to shape subtype evolution which manifested as unique geographic hotspots for each subtype at the global scale. This study reveals how a diversity of avian hosts contribute to viral spread and spillover with the potential to improve surveillance in an era of rapid global change.
Gulls are ubiquitous in urban areas due to a growing reliance on anthropogenic feeding sites, which has led to changes in their abundance, distribution, and migration ecology, with implications for disease transmission. Gulls offer a valuable model for testing hypotheses regarding the dynamics of influenza A virus (IAV) – for which gulls are a natural reservoir in urban areas. We sampled sympatric populations of Ring‐billed (Larus delawarensis), Herring (L. argentatus), and Great Black‐backed Gulls (L. marinus) along the densely populated Atlantic rim of North America to understand how IAV transmission is influenced by drivers such as annual cycle, host species, age, habitat type, and their interplay. We found that horizontal transmission, rather than vertical transmission, played an outsized role in the amplification of IAV due to the convergence of gulls from different breeding grounds and age classes. We detected overlapping effects of age and season in our prevalence model, identifying juveniles during autumn as the primary drivers of the seasonal epidemic in gulls. Gulls accumulated immunity over their lifespan, however short‐term fluctuations in seroprevalence were observed, suggesting that migration may impose limits on the immune system to maintain circulating antibodies. We found that gulls in coastal urban habitats had higher viral prevalence than gulls captured inland, correlating with higher richness of waterbird species along the coast, a mechanism supported by our movement data. The peak in viral prevalence in newly fledged gulls that are capable of long‐distance movement has important implications for the spread of pathogens to novel hosts during the migratory season as well as for human health as gulls increasingly utilize urban habitats.
The age of an animal, determined by time (chronological age) as well as genetic and environmental factors (biological age), influences the likelihood of mortality and reproduction and thus the animal’s contribution to population growth. For many long-lived species, such as bats, a lack of external and morphological indicators has made determining age a challenge, leading researchers to examine genetic markers of age for application to demographic studies. One widely studied biomarker of age is telomere length, which has been related both to chronological and biological age across taxa, but only recently has begun to be studied in bats. We assessed telomere length from the DNA of known-age and minimum known-age individuals of two bat species using a quantitative PCR assay. We determined that telomere length was quadratically related to chronological age in big brown bats (Eptesicus fuscus), although it had little predictive power for accurate age determination of unknown-age individuals. The relationship was different in little brown bats (Myotis lucifugus), where telomere length instead was correlated with biological age, apparently due to infection and wing damage associated with white-nose syndrome. Furthermore, we showed that wing biopsies currently are a better tissue source for studying telomere length in bats than guano and buccal swabs; the results from the latter group were more variable and potentially influenced by storage time. Refinement of collection and assessment methods for different non-lethally collected tissues will be important for longitudinal sampling to better understand telomere dynamics in these long-lived species. Although further work is needed to develop a biomarker capable of determining chronological age in bats, our results suggest that biological age, as reflected in telomere length, may be influenced by extrinsic stressors such as disease.
The patterns of recovery from injury or infection are not well studied in free-ranging animals. Bats that survive the fungal disease white-nose syndrome (WNS) often emerge from hibernation suffering from skin infections and wing damage. The extent of wing damage reflects physiological and immunological responses to WNS and may impact the ability of bats to fly, forage, and reproduce. Here, we built on previous studies of wing damage in both captive and free-ranging bats to better understand the patterns and extent of wing damage healing in little brown bats (Myotis lucifugus) post-hibernation. We quantified two main types of wing damage, black necrotic dots and white spots, and used the extent of damage to assign bats 1 of 6 wing damage scores. We found that the patterns of black dots and white spots on wing membranes of free-ranging bats aligned with the patterns observed in captive bats soon after emergence from hibernation. Black dot extent was highest at the beginning of the active season in May, while white spot extent peaked 3–4 weeks later. Our study also extends our knowledge of wing damage healing throughout the active season. Wing scores of bats recaptured within the summer decreased or stayed the same and >95% had negligible signs of wing damage by August. We found that black dots were more indicative of disease status than other types of wing damage and could be consistently quantified in the field and from photographs by multiple observers. These results suggest that black dots and our wing damage scoring system can be used to better understand the patterns of post-hibernation healing in little brown bats impacted by WNS.
Careers in biology are often motivated by a love for wildlife and the outdoors, and a fascination with the processes and mechanisms that gave rise to life, its diversity, and the patterns that emerge within its complexity. Yet during the unprecedented times of the COVID-19 pandemic, with its lockdowns and isolation, many of us have taken the time to reflect and realize that the most meaningful aspects of our careers are the connections we make through our science and the positive impact that we can have on others. Thomas Kunz was an admirable example of a biologist who not only made substantial contributions to science and bat conservation but also positively affected the lives of students he mentored and the collaborators with whom he worked. On the oneyear anniversary of his death, we reflect on Tom's impact and pay tribute to his personal and scientific legacy. First, we briefly summarize the major highlights of Tom's life and career. Then, we reflect on the diverse ways Tom has impacted our lives both personally and scientifically.
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