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Research products from students and faculty in the Center.  Student co-authors are indicated with (§) for undergraduates and (‡) for graduates; postdocs are indicated by (*).

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Marshall, B.M., P. Freed, L.J. Vitt, P. Bernardo, G. Vogel, S. Lotzkat, M. Franzen, J. Hallermann, R.D. Sage, B. Bush, M.R. Duarte, L.J. Avila, D. Jandzik, B. Klusmeyer, B. Maryan, J. Hošek, and P. Uetz (2020) An inventory of online reptile images. Zootaxa 4896:251-264.

No central online repository exists for the collection of animal images; hence it remains unclear how extensively species have been illustrated in the published literature or online. Here we compiled a list of more than 8000 reptile species (out of 11,341) that have photos in one of six popular online repositories, namely iNaturalist (6,349 species), the Reptile Database (5,144), Flickr (4,386), CalPhotos (3,071), Wikimedia (2,952), and Herpmapper (2,571). These sites have compiled over one million reptile photos, with some species represented by tens of thousands of images. Despite the number of images, many species have only one or a few images. This suggests that a considerable fraction of morphological and geographic variation is under documented or difficult to access. We highlight prominent gaps in amphisbaenians, lizards, and snakes, with geographic hotspots for species without images in Central Africa, Pacific Islands, and the Andes Mountains. We present a list of ~3,000 species without photos in any of the six databases and ask the community to fill the gaps by depositing images on one of these sites (preferably with minimal copyright restrictions).

Tassone, E.E., L.S. Miles, R.J. Dyer, M.S. Rosenberg, R.M. Cowling, and B.C. Verrelli (2021) Evolutionary stability, landscape heterogeneity, and human land-usage shape population genetic connectivity in the Cape Floristic Region biodiversity hotspot. Evolutionary Applications 14:in press.

As human‐induced change eliminates natural habitats, it impacts genetic diversity and population connectivity for local biodiversity. The South African Cape Floristic Region (CFR) is the most diverse extratropical area for plant biodiversity, and much of its habitat is protected as a UNESCO World Heritage site. There has long been great interest in explaining the underlying factors driving this unique diversity, especially as much of the CFR is endangered by urbanization and other anthropogenic activity. Here, we use a population and landscape genetic analysis of SNP data from the CFR endemic plant Leucadendron salignum or “common sunshine conebush” as a model to address the evolutionary and environmental factors shaping the vast CFR diversity. We found that high population structure, along with relatively deeper and older genealogies, are characteristic of the southwestern CFR, whereas, low population structure and more recent lineage coalescence depicts the eastern CFR. Population network analyses show genetic connectivity is facilitated in areas of lower elevation and higher seasonal precipitation. These population genetic signatures corroborate CFR species‐level patterns consistent with high Pleistocene biome stability and landscape heterogeneity in the southwest, but with coincident instability in the east. Finally, we also find evidence of human land‐usage as a significant gene flow barrier, especially in severely‐threatened lowlands where genetic connectivity has been historically the highest. These results help identify areas where conservation plans can prioritize protecting high genetic diversity threatened by contemporary human activities within this unique cultural UNESCO site.

Puccio, T., K.S. Kunka, B. Zhu, P. Xu, and T. Kitten (2020) Manganese depletion leads to multisystem changes in the transcriptome of the opportunistic pathogen Streptococcus sanguinis. Frontiers in Microbiology 11:592615.

Streptococcus sanguinis is a primary colonizer of teeth and is typically considered beneficial due to its antagonistic relationship with the cariogenic pathogen Streptococcus mutans. However, S. sanguinis can also act as an opportunistic pathogen should it enter the bloodstream and colonize a damaged heart valve, leading to infective endocarditis. Studies have implicated manganese acquisition as an important virulence determinant in streptococcal endocarditis. A knockout mutant lacking the primary manganese import system in S. sanguinis, SsaACB, is severely attenuated for virulence in an in vivo rabbit model. Manganese is a known cofactor for several important enzymes in S. sanguinis, including superoxide dismutase, SodA, and the aerobic ribonucleotide reductase, NrdEF. To determine the effect of manganese depletion on S. sanguinis, we performed transcriptomic analysis on a ΔssaACB mutant grown in aerobic fermentor conditions after the addition of the metal chelator EDTA. Despite the broad specificity of EDTA, analysis of cellular metal content revealed a decrease in manganese, but not in other metals, that coincided with a drop in growth rate. Subsequent supplementation with manganese, but not iron, zinc, or magnesium, restored growth in the fermentor post-EDTA. Reduced activity of Mn-dependent SodA and NrdEF likely contributed to the decreased growth rate post-EDTA, but did not appear entirely responsible. With the exception of the Dps-like peroxide resistance gene, dpr, manganese depletion did not induce stress response systems. By comparing the transcriptome of ΔssaACB cells pre- and post-EDTA, we determined that manganese deprivation led to altered expression of diverse systems. Manganese depletion also led to an apparent induction of carbon catabolite repression in a glucose-independent manner. The combined results suggest that manganese limitation produces effects in S. sanguinis that are diverse and complex, with no single protein or system appearing entirely responsible for the observed growth rate decrease. This study provides further evidence for the importance of this trace element in streptococcal biology. Future studies will focus on determining mechanisms for regulation, as the multitude of changes observed in this study indicate that multiple regulators may respond to manganese levels.

Zhu, B, S.P. Green, X. Ge, T. Puccio, H. Nadhem, H. Ge, L. Bao, T. Kitten, and P. Xu (2020) Genome-wide identification of Streptococcus sanguinis fitness genes in human serum and discovery of potential selective drug targets. Molecular Microbiology in press:.

Streptococcus sanguinis is a primary colonizer of teeth and is associated with oral health. When it enters the bloodstream, however, this bacterium may cause the serious illness infective endocarditis. The genes required for survival and proliferation in blood have not been identified. The products of these genes could provide a rich source of targets for endocarditis‐specific antibiotics possessing greater efficacy for endocarditis, and also little or no activity against those bacteria that remain in the mouth. We previously created a comprehensive library of S. sanguinis mutants lacking every nonessential gene. We have now screened each member of this library for growth in human serum and discovered 178 mutants with significant abundance changes. The main biological functions disrupted in these mutants, including purine metabolism, were highlighted via network analysis. The components of an ECF‐family transporter were required for growth in serum and were shown for the first time in any bacterium to be essential for endocarditis virulence. We also identified two mutants whose growth was reduced in serum but not in saliva. This strategy promises to enable selective targeting of bacteria based on their location in the body, in this instance, treating or preventing endocarditis while leaving the oral microbiome intact.

Farooq, H. and P. Uetz (2020) Identifying Australian snakes by color patterns. Vertebrate Zoology 70:473-482.

We investigated if Australian snakes can be identified by using their color, pattern, size and location. We coded these criteria for the 185 terrestrial snake species of Australia (excluding 37 species of sea snakes from our analysis). Uniformly brown snakes are most common, followed by banded and blotched species. Some highly variable species can have dozens of color patterns. For most localities these four criteria are sufficient to narrow down the number of possible species to fewer than 21 species and in most cases accurate identification is possible with a few photos for comparison. Given that most Australian snakes are venomous, accurately identifying snakes is also of medical importance. In addition to identifying snakes, colors and patterns provide useful data for phylogenetic and ecological studies.

Alberti, M, E.P. Palkovacs, S. Des Roches, L. De Meester, K.I. Brans, L. Govaert, N.B. Grimm, N.C. Harris, A.P. Hendry, C.J. Schell, M. Szulkin, J. Munshi-South, M.C. Urban, and B.C. Verrelli (2020) The complexity of urban eco-evolutionary dynamics. Bioscience 70:772-793.

Urbanization is changing Earth’s ecosystems by altering the interactions and feedbacks between the fundamental ecological and evolutionary processes that maintain life. Humans in cities alter the eco-evolutionary play by simultaneously changing both the actors and the stage on which the eco-evolutionary play takes place. Urbanization modifies land surfaces, microclimates, habitat connectivity, ecological networks, food webs, species diversity, and species composition. These environmental changes can lead to changes in phenotypic, genetic, and cultural makeup of wild populations that have important consequences for ecosystem function and the essential services that nature provides to human society, such as nutrient cycling, pollination, seed dispersal, food production, and water and air purification. Understanding and monitoring urbanization-induced evolutionary changes is important to inform strategies to achieve sustainability. In the present article, we propose that understanding these dynamics requires rigorous characterization of urbanizing regions as rapidly evolving, tightly coupled human–natural systems. We explore how the emergent properties of urbanization affect eco-evolutionary dynamics across space and time. We identify five key urban drivers of change—habitat modification, connectivity, heterogeneity, novel disturbances, and biotic interactions—and highlight the direct consequences of urbanization-driven eco-evolutionary change for nature’s contributions to people. Then, we explore five emerging complexities—landscape complexity, urban discontinuities, socio-ecological heterogeneity, cross-scale interactions, legacies and time lags—that need to be tackled in future research. We propose that the evolving metacommunity concept provides a powerful framework to study urban eco-evolutionary dynamics.

Des Roches, S., K.I. Brans, M. Lambert, L.R. Rivkin, A. Savage, C.J. Schell, C. Correa, L. De Meester, S.E. Diamond, L. Govaert, N.B. Grimm, N.C. Harris, A.P. Hendry, M.T.J. Johnson, J. Munshi-South, E.P. Palkovacs, M. Szulkin, M.C. Urban, B.C. Verrelli, and M. Alberti (2020) Socio-eco-evolutionary dynamics in cities. Evolutionary Applications in press:.

Cities are uniquely complex systems regulated by interactions and feedbacks between natural and social processes. Characteristics of human society – including culture, economics, technology, and politics – underlie social patterns and activity, creating a heterogeneous environment that can influence and be influenced by both ecological and evolutionary processes. Increasing interest in urban ecology and evolutionary biology has coincided with growing interest in eco‐evolutionary dynamics, which encompasses the interactions and reciprocal feedbacks between evolution and ecology. Research on both urban evolutionary biology and eco‐evolutionary dynamics frequently focuses on contemporary evolution of species that have potentially substantial ecological – and even social – significance. Still, little research fully integrates urban evolutionary biology and eco‐evolutionary dynamics, and rarely do researchers in either of these fields fully consider the role of human social patterns and processes. Because cities are fundamentally regulated by human activities, are inherently interconnected, and are frequently undergoing social and economic transformation, they represent an opportunity for ecologists and evolutionary biologists to study urban “socio‐eco‐evolutionary dynamics.” Through this new framework, we encourage researchers of urban ecology and evolution to fully integrate human social drivers and feedbacks to increase understanding and conservation of ecosystems, their functions, and their contributions to people within and outside cities.

Monteiro, E.F., C. Fernandez-Becerra, M.S. Araujo, M.R. Messias, L.S. Ozaki, A.M. Ribeiro de Castro Duarte, M.G. Bueno, J.L. Catao-Dias, C.R. Fernandes Chagas, B.S. Mathias, M. Gomes dos Santos, S.V. Santos, M.M. Holcman, J.C. Souza Jr., and K. Kirchgatter (2020) Naturally acquired humoral immunity against malaria parasites in non-human primates from the Brazilian Amazon, Cerrado and Atlantic Forest. Pathogens 9:525.

Non-human primates (NHPs) have been shown to be infected by parasites of the genus Plasmodium, the etiological agent of malaria in humans, creating potential risks of zoonotic transmission. Plasmodium brasilianum, a parasite species similar to P. malariae of humans, have been described in NHPs from Central and South America, including Brazil. The merozoite surface protein 1 (MSP1), besides being a malaria vaccine candidate, is highly immunogenic. Due to such properties, we tested this protein for the diagnosis of parasite infection. We used recombinant proteins of P. malariae MSP1, as well as of P. falciparum and P. vivax, for the detection of antibodies anti-MSP1 of these parasite species, in the sera of NHPs collected in different regions of Brazil. About 40% of the NHP sera were confirmed as reactive to the proteins of one or more parasite species. A relatively higher number of reactive sera was found in animals from the Atlantic Forest than those from the Amazon region, possibly reflecting the former more intense parasite circulation among NHPs due to their proximity to humans at a higher populational density. The presence of Plasmodium positive NHPs in the surveyed areas, being therefore potential parasite reservoirs, needs to be considered in any malaria surveillance program.

Rosenberg, M.S. (2020) A fresh look at the biodiversity lexicon for fiddler crabs (Decapoda: Brachyura: Ocypodidae). Part 2: Biogeography. Journal of Crustacean Biology 40:364-383.

Fiddler crabs (Ocypodidae Rafinesque, 1815) occupy most tropical and semitropical coastlines worldwide where they are keystone species and ecosystem engineers. I present updated ranges for all 105 species and explore both global and local patterns to establish a baseline distribution as species ranges begin to shift with climate change. Globally, the average number of species per occupied coastline is five, with only limited allopatry observed within the group. Cohesive species assemblages were used to define four zoogeographic fiddler realms containing 24 provinces and transitional zones. These regions can serve as units of study when trying to explore which factors influence the distribution of coastal species.

Garg, A., D. Leipe, and P. Uetz (2019) The disconnect between DNA and species names: Lessons from reptile species in the NCBI taxonomy database. Zootaxa 4706:401-407.

We compared the species names in the Reptile Database, a dedicated taxonomy database, with those in the NCBI taxonomy database, which provides the taxonomic backbone for the GenBank sequence database. About 67% of the known ~11,000 reptile species are represented with at least one DNA sequence and a binary species name in GenBank. However, a common problem arises through the submission of preliminary species names (such as “Pelomedusa sp. A CK-2014”) to GenBank and thus the NCBI taxonomy. These names cannot be assigned to any accepted species names and thus create a disconnect between DNA sequences and species. While these names of unknown taxonomic meaning sometimes get updated, often they remain in GenBank which now contains sequences from ~1,300 such “putative” reptile species tagged by informal names (~15% of its reptile names). We estimate that NCBI/GenBank probably contain tens of thousands of such “disconnected” entries. We encourage sequence submitters to update informal species names after they have been published, otherwise the disconnect will cause increasing confusion and possibly misleading taxonomic conclusions.

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