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Understanding the processes that shape genetic diversity by either promoting or preventing population divergence can help identify geographic areas that either facilitate or limit gene flow. Furthermore, broadly distributed species allow us to understand how biogeographic and ecogeographic transitions affect gene flow. We investigated these processes using genomic data in the Northern Alligator Lizard (Elgaria coerulea), which is widely distributed in Western North America across diverse ecoregions (California Floristic Province and Pacific Northwest) and mountain ranges (Sierra Nevada, Coastal Ranges, and Cascades). We collected single-nucleotide polymorphism data from 120 samples of E. coerulea. Biogeographic analyses of squamate reptiles with similar distributions have identified several shared diversification patterns that provide testable predictions for E. coerulea, including deep genetic divisions in the Sierra Nevada, demographic stability of southern populations, and recent post-Pleistocene expansion into the Pacific Northwest. We use genomic data to test these predictions by estimating the structure, connectivity, and phylogenetic history of populations. At least 10 distinct populations are supported, with mixed-ancestry individuals situated at most population boundaries. A species tree analysis provides strong support for the early divergence of populations in the Sierra Nevada Mountains and recent diversification into the Pacific Northwest. Admixture and migration analyses detect gene flow among populations in the Lower Cascades and Northern California, and a spatial analysis of gene flow identified significant barriers to gene flow across both the Sierra Nevada and Coast Ranges. The distribution of genetic diversity in E. coerulea is uneven, patchy, and interconnected at population boundaries. The biogeographic patterns seen in E. coerulea are consistent with predictions from co-distributed species.

 

Colourful displays are used by diverse taxa to warn predators of dangerous defences (aposematism). Aposematic coloration is especially widespread among amphibians, which are often protected by harmful toxins. Pacific newts (Taricha) are considered a model of aposematism because when threatened, they arch the head and tail upwards to expose a vivid orange ventrum against a dark dorsum. Given that newts are defended by tetrodotoxin (TTX), a lethal neurotoxin, this signal is assumed to warn predators that an attack would be risky. However, colours have not been quantified in Taricha, and it remains unknown whether coloration provides qualitatively honest (signalling toxic defence) or quantitatively honest (signalling toxin level) warnings. We used two colour quantification methods (spectrometry and hyperspectral imaging) to measure chromatic (hue) and achromatic (brightness) qualities of ventral and dorsal coloration in two newt species (Taricha granulosa and Taricha sierrae). We assessed qualitative honesty using visual models of potential predators (snakes, birds and mammals). Next, we evaluated quantitative honesty by measuring TTX in newts and examining the potential correlation between defence level (amount of TTX) and colorimetrics. We found support for qualitative but not quantitative honesty. Selective pressures and evolutionary constraints might impede the evolution of honest quantitative signalling in this system.

 

Research on plant-pollinator interactions requires a diversity of perspectives and approaches, and documenting changing pollinator-plant interactions due to declining insect diversity and climate change is especially challenging. Natural history collections are increasingly important for such research and can provide ecological information across broad spatial and temporal scales. Here, we describe novel approaches that integrate museum specimens from insect and plant collections with field observations to quantify pollen networks over large spatial and temporal gradients. We present methodological strategies for evaluating insect-pollen network parameters based on pollen collected from museum insect specimens. These methods provide insight into spatial and temporal variation in pollen-insect interactions and complement other approaches to studying pollination, such as pollinator observation networks and flower enclosure experiments. We present example data from butterfly pollen networks over the past century in the Great Basin Desert and Sierra Nevada Mountains, United States. Complementary to these approaches, we describe rapid pollen identification methods that can increase speed and accuracy of taxonomic determinations, using pollen grains collected from herbarium specimens. As an example, we describe a convolutional neural network (CNN) to automate identification of pollen. We extracted images of pollen grains from 21 common species from herbarium specimens at the University of Nevada Reno (RENO). The CNN model achieved exceptional accuracy of identification, with a correct classification rate of 98.8%. These and similar approaches can transform the way we estimate pollination network parameters and greatly change inferences from existing networks, which have exploded over the past few decades. These techniques also allow us to address critical ecological questions related to mutualistic networks, community ecology, and conservation biology. Museum collections remain a bountiful source of data for biodiversity science and understanding global change. 

Landscape patterns of phenotypic coevolution are determined by variation in the outcome of predator–prey interactions. These outcomes may depend not only on the functional phenotypes that mediate species interactions, but also on aspects of the environment that enable encounters between coevolutionary partners.

Exploring the relationship between coevolutionary traits and the environment requires extensive sampling across the range of the interaction to determine the relationship between local ecological variation and coevolution.

In this study, we synthesized >30 years of data on predator–prey interactions between toxic newts (Taricha granulosa) and their snake predators (Thamnophis sirtalis) to explore the environmental predictors of arms race escalation.

We found that geographic variation in phenotypes at the interface of coevolution was best predicted by a combination of community and climatic variation. Coevolutionary phenotypes were greatest in environments with climate favourable for newt–snake overlap. We found prey toxicity was elevated in regions with more predator species, and predator resistance was higher in regions with more prey species.

Our results suggest specific environmental conditions reinforce the process of coevolution, signifying the phenotypic outcomes of coevolutionary arms races are sensitive to local ecological contexts that vary across the landscape.

Read the freePlain Language Summaryfor this article on the Journal blog.

 

Antagonistic coevolution between natural enemies can produce highly exaggerated traits, such as prey toxins and predator resistance. This reciprocal process of adaptation and counter‐adaptation may also open doors to other evolutionary novelties not directly involved in the phenotypic interface of coevolution. We tested the hypothesis that predator–prey coevolution coincided with the evolution of conspicuous coloration on resistant predators that retain prey toxins. In western North America, common garter snakes (Thamnophis sirtalis) have evolved extreme resistance to tetrodotoxin (TTX) in the coevolutionary arms race with their deadly prey, Pacific newts (Tarichaspp.). TTX‐resistant snakes can retain large amounts of ingested TTX, which could serve as a deterrent against the snakes' own predators if TTX toxicity and resistance are coupled with a conspicuous warning signal. We evaluated whether arms race escalation covaries with bright red coloration in snake populations across the geographic mosaic of coevolution. Snake colour variation departs from the neutral expectations of population genetic structure and covaries with escalating clines of newt TTX and snake resistance at two coevolutionary hotspots. In the Pacific Northwest, bright red coloration fits an expected pattern of an aposematic warning to avian predators: TTX‐resistant snakes that consume highly toxic newts also have relatively large, reddish‐orange dorsal blotches. Snake coloration also seems to have evolved with the arms race in California, but overall patterns are less intuitively consistent with aposematism. These results suggest that interactions with additional trophic levels can generate novel traits as a cascading consequence of arms race coevolution across the geographic mosaic.

 

Reciprocal adaptation is the hallmark of arms race coevolution. Local coadaptation between natural enemies should generate a geographic mosaic pattern where both species have roughly matched abilities across their shared range. However, mosaic variation in ecologically relevant traits can also arise from processes unrelated to reciprocal selection, such as population structure or local environmental conditions. We tested whether these alternative processes can account for trait variation in the geographic mosaic of arms race coevolution between resistant garter snakes (Thamnophis sirtalis) and toxic newts (Taricha granulosa). We found that predator resistance and prey toxin levels are functionally matched in co-occurring populations, suggesting that mosaic variation in the armaments of both species results from the local pressures of reciprocal selection. By the same token, phenotypic and genetic variation in snake resistance deviates from neutral expectations of population genetic differentiation, showing a clear signature of adaptation to local toxin levels in newts. Contrastingly, newt toxin levels are best predicted by genetic differentiation among newt populations, and to a lesser extent, by the local environment and snake resistance. Exaggerated armaments suggest that coevolution occurs in certain hotspots, but prey population structure seems to be of particular influence on local phenotypic variation in both species throughout the geographic mosaic. Our results imply that processes other than reciprocal selection, like historical biogeography and environmental pressures, represent an important source of variation in the geographic mosaic of coevolution. Such a pattern supports the role of “trait remixing” in the geographic mosaic theory, the process by which non-adaptive forces dictate spatial variation in the interactions among species.

 

A central aim of biogeography is to understand how biodiversity is generated and maintained across landscapes. Here, we establish phylogenetic and population genetic patterns in a widespread reptile to quantify the influence of historical biogeography and current environmental variation on patterns of genetic diversity.

Western North America.

Western terrestrial garter snake,Thamnophis elegans.

We used double‐digest RADseq to estimate phylogenetic relationships and characterize population genetic structure across the three widespread subspecies ofT. elegans:T. e. vagrans(wandering garter snake),T. e. elegans(mountain garter snake) andT. e. terrestris(coast garter snake). We assessed patterns of dispersal and vicariance across biogeographic regions using ancestral area reconstruction (AAR) and deviations from isolation‐by‐distance across the landscape using estimated effective migration surfaces (EEMS). We identified environmental variables potentially shaping local adaptation in regional lineages using genetic‐environment association (GEA) analyses.

We recovered three well‐differentiated genetic groups that correspond to the three subspecies. AAR analyses inferred the eastern Cascade Range as the ancestral area, with dispersal to both the east and west across western North America. Populations ofT. e. elegansdisplayed a latitudinal gradient in genetic variation across the Sierra Nevada and northern California, while populations ofT. e. terrestrisshow discrete genetic breaks consistent with well‐known biogeographic barriers. Lastly, GEA analyses identified allele frequency shifts at loci associated with a common set of environmental variables in bothT. e. elegansandT. e. terrestris.

T. elegansis composed of distinct evolutionary lineages, each with its own geographic range and history of diversification.T. e. elegansandT. e. terrestrisshow unique patterns of diversification as populations dispersed from east to west and while adapting to the new environments they colonized. Historical events, landscape features and environmental variation have all contributed to patterns of differentiation inT. elegans.

 

Trait specialization often comes at the expense of original trait function, potentially causing evolutionary tradeoffs that may render specialist populations vulnerable to extinction. However, many specialized adaptations evolve repeatedly, suggesting selection favors specialization in specific environments. Some garter snake (Thamnophis) populations possess specialized mutations in voltage‐gated sodium channels that allow them to consume Pacific newts (Taricha) defended by a highly potent neurotoxin (tetrodotoxin). These mutations, however, also decrease protein and muscle function, suggesting garter snakes may suffer evolutionary tradeoffs. We measured a key physiological process, standard metabolic rate (SMR), to investigate whether specialized adaptations in toxin‐resistant garter snakes affect baseline energy expenditure. In snakes, skeletal muscles influence metabolism and power ventilation, so inefficiencies of sodium channels in these muscles might impact whole‐animal energy expenditure. Further, because sodium channels are membrane‐bound proteins, inefficiencies of channel kinetics and performance might be exacerbated at suboptimal temperatures. We measured SMR in 2 species,Thamnophis atratusandThamnophis sirtalis, that independently evolved tetrodotoxin resistance through unique mutations, providing replicate experiments with distinct underlying genetics and potential physiological costs. Despite our expectations, neither resistance phenotype nor sodium channel genotype affected metabolism and resistant snakes did not perform worse under suboptimal body temperature. Instead,T. atratusandT. sirtalisshow nearly identical rates of mass‐adjusted energy expenditure at both temperatures, despite differing eco‐morphologies, life histories, and distant phylogenetic positions. These findings suggest SMR may be a conserved feature ofThamnophis, and that any organismal tradeoffs may be compensated to retain whole‐animal function.