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Exploiting the physiology of lampreys to refine methods of control and conservation

Lampreys (order: Petromyzontiformes) represent one of two extant groups of jawless fishes, also called cyclostomes. Lampreys have a variety of unique features that distinguish them from other fishes. Here we review the physiological features of lampreys that have contributed to their evolutionary and ecological success. The term physiology is used broadly to also include traits involving multiple levels of biological organization, like swimming performance, that have a strong but not exclusively physiological basis. We also provide examples of how sea lamprey traits are currently being used or investigated to control invasive populations in the Great Lakes, such as reduced capacity to detoxify lampricides, inability to surmount low barriers or dams, and sensitivity to several lamprey-specific chemosensory pheromones and alarm cues. Specific suggestions are also provided for how an improved knowledge of lamprey physiological traits could be exploited for more effective conservation of native lampreys and lead to the development of next generation sea lamprey control and conservation tools.

Journal of Great Lakes Research↗

Replicated landscape genomics identifies evidence of local adaptation to urbanization in wood frogs

Native species that persist in urban environments may benefit from local adaptation to novel selection factors. We used double-digest restriction-side associated DNA (RAD) sequencing to evaluate shifts in genome-wide genetic diversity and investigate the presence of parallel evolution associated with urban-specific selection factors in wood frogs ( Lithobates sylvaticus ). Our replicated paired study design involved 12 individuals from each of 4 rural and urban populations to improve our confidence that detected signals of selection are indeed associated with urbanization. Genetic diversity measures were less for urban populations; however, the effect size was small, suggesting little biological consequence. Using an F ST outlier approach, we identified 37 of 8344 genotyped single nucleotide polymorphisms with consistent evidence of directional selection across replicates. A genome-wide association study analysis detected modest support for an association between environment type and 12 of the 37 F ST outlier loci. Discriminant analysis of principal components using the 37 F ST outlier loci produced correct reassignment for 87.5% of rural samples and 93.8% of urban samples. Eighteen of the 37 F ST outlier loci mapped to the American bullfrog ( Rana [Lithobates] catesbeiana ) genome, although none were in coding regions. This evidence of parallel evolution to urban environments provides a powerful example of the ability of urban landscapes to direct evolutionary processes.

Maine↗

Individual heterogeneity in growth and age at sexual maturity: A gamma process analysis of capture–mark–recapture data

Knowledge of organisms’ growth rates and ages at sexual maturity is important for conservation efforts and a wide variety of studies in ecology and evolutionary biology. However, these life history parameters may be difficult to obtain from natural populations: individuals encountered may be of unknown age, information on age at sexual maturity may be uncertain and interval-censored, and growth data may include both individual heterogeneity and measurement errors. We analyzed mark–recapture data for Red-backed Salamanders ( Plethodon cinereus ) to compare sex-specific growth rates and ages at sexual maturity. Aging of individuals was made possible by the use of a von Bertalanffy model of growth, complemented with models for interval-censored and imperfect observations at sexual maturation. Individual heterogeneity in growth was modeled through the use of Gamma processes. Our analysis indicates that female P. cinereus mature earlier and grow more quickly than males, growing to nearly identical asymptotic size distributions as males.

Journal of Agricultural, Biological, and Environme↗

Understanding the genetic effects of recent habitat fragmentation in the context of evolutionary history: Phylogeography and landscape genetics of a southern California endemic Jerusalem cricket (Orthoptera: Stenopelmatidae: Stenopelmatus)

Habitat loss and fragmentation due to urbanization are the most pervasive threats to biodiversity in southern California. Loss of habitat and fragmentation can lower migration rates and genetic connectivity among remaining populations of native species, reducing genetic variability and increasing extinction risk. However, it may be difficult to separate the effects of recent anthropogenic fragmentation from the genetic signature of prehistoric fragmentation due to previous natural geological and climatic changes. To address these challenges, we examined the phylogenetic and population genetic structure of a flightless insect endemic to cismontane southern California, Stenopelmatus 'mahogani' (Orthoptera: Stenopelmatidae). Analyses of mitochondrial DNA sequence data suggest that diversification across southern California began during the Pleistocene, with most haplotypes currently restricted to a single population. Patterns of genetic divergence correlate with contemporary urbanization, even after correcting for (geographical information system) GIS-based reconstructions of fragmentation during the Pleistocene. Theoretical simulations confirm that contemporary patterns of genetic structure could be produced by recent urban fragmentation using biologically reasonable assumptions about model parameters. Diversity within populations was positively correlated with current fragment size, but not prehistoric fragment size, suggesting that the effects of increased drift following anthropogenic fragmentation are already being seen. Loss of genetic connectivity and diversity can hinder a population's ability to adapt to ecological perturbations commonly associated with urbanization, such as habitat degradation, climatic changes and introduced species. Consequently, our results underscore the importance of preserving and restoring landscape connectivity for long-term persistence of low vagility native species. Journal compilation ?? 2006 Blackwell Publishing Ltd.

Molecular Ecology↗

Seasonal variations in ectotherm growth rates: Quantifying growth as an intermittent non steady state compensatory process

Generally, growth rates of living organisms are considered to be at steady state, varying only under environmental forcing factors. For example, these rates may be described as a function of light for plants or organic food resources for animals and these could be regulated (or not) by temperature or other conditions. But, what are the consequences for an individual's growth (and also for the population growth) if growth rate variations are themselves dynamic and not steady state? For organisms presenting phases of dormancy or long periods of stress, this is a crucial question. A dynamic perspective for quantifying short-term growth was explored using the daily growth record of the scallop Pecten maximus (L.). This species is a good biological model for ectotherm growth because the shell records growth striae daily. Independently, a generic mathematical function representing the dynamics of mean daily growth rate (MDGR) was implemented to simulate a diverse set of growth patterns. Once the function was calibrated with the striae patterns, the growth rate dynamics appeared as a forced damped oscillation during the growth period having a basic periodicity during two transitory phases (mean duration 43. days) and appearing at both growth start and growth end. This phase is most likely due to the internal dynamics of energy transfer within the organism rather than to external forcing factors. After growth restart, the transitory regime represents successive phases of over-growth and regulation. This pattern corresponds to a typical representation of compensatory growth, which from an evolutionary perspective can be interpreted as an adaptive strategy to coping with a fluctuating environment.

Journal of Sea Research↗

Incubation temperature, developmental biology, and the divergence of sockeye salmon ( Oncorhynchus nerka ) within Lake Washington

Sockeye salmon ( Oncorhynchus nerka) introduced into Lake Washington in the 1930s and 1940s now spawn at several different sites and over a period of more than 3 months. To test for evolutionary divergence within this derived lineage, embryos that would have incubated in different habitats (Cedar River or Pleasure Point Beach) or at different times (October, November, or December in the Cedar River) were reared in the laboratory at 5, 9, and 12.5??C. Some developmental variation mirrored predictions of adaptive divergence: (i) survival at 12.5??C was highest for embryos most likely to experience such temperatures in the wild (Early Cedar), (ii) development rate was fastest for progeny of late spawners (Late Cedar), and (iii) yolk conversion efficiency was matched to natural incubation temperatures. These patterns likely had a genetic basis because they were observed in a common environment and could not be attributed to differences in egg size. The absolute magnitude of divergence in development rates was moderate (Late Cedar embryos emerged only 6 days earlier at 9??C) and some predictions regarding development rates were not supported. Nonetheless our results provide evidence of adaptive divergence in only 9-14 generations.

Washington↗

Directional selection shifts trait distributions of planted species in dryland restoration

The match between species trait values and local abiotic filters can restrict community membership. An often-implicit assumption of this relationship is that abiotic filters select for a single locally optimal strategy, though difficulty in isolating effects of the abiotic environment from those of dispersal limitation and biotic interactions has resulted in few empirical tests of this assumption. Similar constraints have made it difficult to assess whether the type and intensity of abiotic filters shift along gradients of environmental harshness, as predicted by the stress-dominance hypothesis. We planted 9,216 plants of 29 perennial grass and forb species that had a range of functional trait values and were assigned to a warm, intermediate or cool temperature tolerance pool across eight sites on the Colorado Plateau. We compared the distributions of traits of surviving individuals to null distributions to evaluate whether there were shifts in trait means and variation. Borrowing from phenotypic selection concepts in evolutionary biology, we assessed support for stabilizing, directional and disruptive abiotic filtering of trait distributions and whether these types of filtering varied with initial species pool. Functional composition was significantly different from null distributions for nearly all traits at all sites, with trait variation more restricted in harsher abiotic conditions, supporting the stress-dominance hypothesis. Contrary to expectations, we primarily found evidence for directional selection, which increased in frequency in warm species pools while disruptive selection was found more often in cool and intermediate species pools. Synthesis . This study provides a controlled experimental approach to test the effect of the abiotic environment on plant trait filtering. We found that opportunistic strategies allowing for rapid water acquisition during favourable periods improved survival at warmer sites. Species with these strategies may be expected to benefit from increasing aridity and may be selected for active management efforts. More generally, the prevalence of directional selection may have important implications for dynamic vegetation models that rely on trait distributions for translating environmental variation into ecosystem processes.

Journal of Ecology↗

The chromosomes of the Didelphidae (Marsupialia) and their evolutionary significance

One hundred and seventy-seven specimens of American didelphids, representing 9 genera and 22 species have been studied for their chromosomal constitution. Didelphids are very conservative in chromosomal complements. All of the studied species can be sorted into one of three kinds of karyotypes: 2 n = 14 (three species of Didelphis, one of Lutreolina, two of Philander, and one of Chironectes) , 2 n = 14 (eight species of Marmosa, one of Metachirus, three of Caluromys, and one of Dromiciops), and 2 n = 18 (three species of Monodelphis). These karyotypes are stable, showing only minor variations within each basic pattern. It is concluded that chromosomals evolution in the Didelphidae proceededs from low numbers to higher numbers by a process of centromeric fissioning complemented by some pericentric inversions and/or translocations. The pattern of karyotypic stability is consistent with bradytely at the organismic level of evolution. This is explained by a low rate of regulatory genetic evolution promoted by epistatic selection favouring the retention of chromosomal arrangements highly advantageous for overall adaptation.

Biological Journal of the Linnean Society↗

Global review reveals how disparate study motivations, analytical designs, and focal ions limit understanding of salinization effects on freshwater animals

Global salinization of freshwaters is adversely affecting biotic communities and ecosystem processes. We reviewed six decades (1960–2020) of literature published on animal responses to increased salinities across different taxonomic and ecological contexts and identified knowledge gaps. From 585 journal articles, we characterized 5924 responses of mollusks, crustaceans, zooplankton, non-arthropod invertebrates (NAI), insects, fishes, and amphibians to salinization. Insects and fishes were the most studied taxa; Na + and Cl − were the most studied ions − . Collectively, concentrations of the ions examined typically spanned five orders of magnitude. Species' invasiveness was a key motivation for studying mollusks, crustaceans, and fishes; threats of urbanization and road salts were key motivations for studying NAI, zooplankton, and amphibians. Laboratory studies were more common than field studies for most taxa. Focal life stages in laboratory studies varied widely but juveniles and adults were represented similarly in field studies. Studies of mollusks, NAI, and crustacean focused on adults; studies of zooplankton, insects, fishes, and amphibians focused on juveniles. Organismal- and population-level responses measuring solute uptake, internal chemistry, body condition, or ion concentrations predominated laboratory studies; population- and assemblage-level responses measuring abundance, spatial distribution, or assemblage composition predominated field studies. Negative responses to salinization predominated but positive and unimodal responses were apparent across all taxa and organizational levels. Key topics for further research include a) salinity responses by more taxa, b) responses to especially toxic ions (i.e., potassium, bicarbonate, sulfate, magnesium), c) mechanisms causing positive and unimodal responses, d) traits underpinning responses, e) effects transcending organizational levels, f) ion-specific response thresholds, and g) interactions between salinity and other stressors. Our review suggests inter-taxa variation in sensitivity to salinization reflects occurrence of certain biological traits, including gill-breathing, semi-permeable skin, multiple life stages, and limited mobility. We propose a traits-based framework to predict salinization sensitivity from shared traits. This evolutionary approach could inform management aimed at preventing or reducing adverse impacts of freshwater salinization.

Science of the Total Environment↗

Challenge to the model of lake charr evolution: Shallow- and deep-water morphs exist within a small postglacial lake

All examples of lake charr ( Salvelinus namaycush ) diversity occur within the largest, deepest lakes of North America (i.e. > 2000 km 2 ). We report here Rush Lake (1.3 km 2 ) as the first example of a small lake with two lake charr morphs (lean and huronicus). Morphology, diet, life history, and genetics were examined to demonstrate the existence of morphs and determine the potential influence of evolutionary processes that led to their formation or maintenance. Results showed that the huronicus morph, caught in deep-water, had a deeper body, smaller head and jaws, higher eye position, greater buoyancy, and deeper peduncle than the shallow-water lean morph. Huronicus grew slower to a smaller adult size, and had an older mean age than the lean morph. Genetic comparisons showed low genetic divergence between morphs, indicating incomplete reproductive isolation. Phenotypic plasticity and differences in habitat use between deep and shallow waters associated with variation in foraging opportunities seems to have been sufficient to maintain the two morphs, demonstrating their important roles in resource polymorphism. Rush Lake expands previous explanations for lake charr intraspecific diversity, from large to small lakes and from reproductive isolation to the presence of gene flow associated with strong ecological drivers.

Biological Journal of the Linnean Society↗

Phylogenetic conservatism in plant phenology

Phenological events – defined points in the life cycle of a plant or animal – have been regarded as highly plastic traits, reflecting flexible responses to various environmental cues. The ability of a species to track, via shifts in phenological events, the abiotic environment through time might dictate its vulnerability to future climate change. Understanding the predictors and drivers of phenological change is therefore critical. Here, we evaluated evidence for phylogenetic conservatism – the tendency for closely related spe-cies to share similar ecological and biological attributes – in phenological traits across flowering plants. We aggregated published and unpublished data on timing of first flower and first leaf, encompassing ~4000 species at 23 sites across the Northern Hemisphere. We reconstructed the phylogeny for the setof included species, first, using the software program Phylomatic, and second, from DNA data. We then quantified phylogenetic conservatism in plant phenology within and across sites. We show that more closely related species tend to flower and leaf at similar times. By contrastingmean flowering times within and across sites, however, we illustrate that it is not the time of yearthat is conserved, but rather the phenological responses to a common set of abiotic cues. Our findings suggest that species cannot be treated as statistically independent when modelling phenological responses. Synthesis. Closely related species tend to resemble each other in the timing of their life-history events, a likely product of evolutionarily conser ved responses to environmental cues. The search for the underlying drivers of phenology must therefore account for species’ shared evolutionary histories.

Journal of Ecology↗

Latitudinal patterns of alien plant invasions

Latitudinal patterns of biodiversity have long been a central topic in ecology and evolutionary biology. However, while most previous studies have focused on native species, little effort has been devoted to latitudinal patterns of plant invasions (with a few exceptions based on data from sparse locations). Using the most up‐to‐date worldwide native and alien plant distribution data from 801 regions (including islands), we compared invasion levels (i.e. alien richness/total richness) in the Northern and Southern Hemispheres and across continental regions and islands around the globe. Results from quantile regressions using B‐splines to model nonlinearity showed (1) declining richness with increasing latitude, although the highest alien richness occurs at around 40 degrees in both hemispheres, (2) decreasing invasion levels towards higher latitudes on islands but a unimodal pattern in invasion level in continental regions in each hemisphere, (3) significantly higher invasion levels on islands than in continental regions and (4) a greater variability in invasion levels on islands at low latitudes than on high‐latitude islands. In continental regions, only the mid‐latitudes had high variability with both low and high invasion levels. Our findings identified latitudes with invasion hotspots where management is urgently needed, and latitudes with many areas of low invasions but high conservation potential where prevention of future invasions should be the priority.

Journal of Biogeography↗

Assembly of the largest squamate reference genome to date: The western fence lizard, Sceloporus occidentalis

Spiny lizards (genus Sceloporus ) have long served as important systems for studies of behavior, thermal physiology, dietary ecology, vector biology, speciation, and biogeography. The western fence lizard, Sceloporus occidentalis , is found across most of the major biogeographical regions in the western United States and northern Baja California, Mexico, inhabiting a wide range of habitats, from grassland to chaparral to open woodlands. As small ectotherms, Sceloporus lizards are particularly vulnerable to climate change, and S. occidentalis has also become an important system for studying the impacts of land use change and urbanization on small vertebrates. Here, we report a new reference genome assembly for S. occidentalis , as part of the California Conservation Genomics Project (CCGP). Consistent with the reference genomics strategy of the CCGP, we used Pacific Biosciences HiFi long reads and Hi-C chromatin-proximity sequencing technology to produce a de novo assembled genome. The assembly comprises a total of 608 scaffolds spanning 2,856 Mb, has a contig N50 of 18.9 Mb, a scaffold N50 of 98.4 Mb, and BUSCO completeness score of 98.1% based on the tetrapod gene set. This reference genome will be valuable for understanding ecological and evolutionary dynamics in S. occidentalis , the species status of the California endemic island fence lizard ( S. becki ), and the spectacular radiation of Sceloporus lizards.

California↗

Cloning, expression, cellular distribution, and role in chemotaxis of a C5a receptor in rainbow trout: The first identification of a C5a receptor in a nonmammalian species

C3a, C4a, and C5a anaphylatoxins generated during complement activation play a key role in inflammation. C5a is the most potent of the three anaphylatoxins in eliciting biological responses. The effects of C5a are mediated by its binding to C5a receptor (C5aR, CD88). To date, C5aR has only been identified and cloned in mammalian species, and its evolutionary history remains ill-defined. To gain insights into the evolution, conserved structural domains, and functions of C5aR, we have cloned and characterized a C5aR in rainbow trout, a teleost fish. The isolated cDNA encoded a 350-aa protein that showed the highest sequence similarity to C5aR from other species. Genomic analysis revealed the presence of one continuous exon encoding the entire open reading frame. Northern blot analysis showed significant expression of the trout C5a receptor (TC5aR) message in PBLs and kidney. Flow cytometric analysis showed that two Abs generated against two different areas of the extracellular N-terminal region of TC5aR positively stained the same leukocyte populations from PBLs. B lymphocytes and granulocytes comprised the majority of cells recognized by the anti-TC5aR. More importantly, these Abs inhibited chemotaxis of PBLs toward a chemoattractant fraction purified from complement-activated trout serum. Our data suggest that the split between C5aR and C3aR from a common ancestral molecule occurred before the emergence of teleost fish. Moreover, we demonstrate that the overall structure of C5aR as well as its role in chemotaxis have remained conserved for >300 million years.

Journal of Immunology↗

Genomic data reveal historical introgression and genetic erosion across an imperiled radiation of Caribbean Spondylurus skinks

Understanding how island biodiversity originates and persists is central to evolutionary biology and conservation. Caribbean islands, shaped by repeated cycles of isolation and connectivity, provide a natural laboratory to evaluate how dispersal, divergence, and introgression interact during diversification. Here we use low-coverage whole-genome data from modern and historical specimens of Caribbean Spondylurus skinks, sampling 14 of 17 described species, to reconstruct the evolutionary history and assess current genetic diversity of this insular radiation. Phylogenomic analyses of mitochondrial and nuclear single nucleotide polymorphisms reveal pervasive discordance among gene trees, extensive introgression, and reject a simple stepping-stone model of diversification across the Caribbean. Instead, Spondylurus diversification reflects repeated long-distance dispersal, gene flow following divergence, and persistence on small islands and cays. Genomic patterns of diversity, runs of homozygosity, effective population sizes, and genetic loads show strong contrasts among species with different recent demographic histories, including severe inbreeding, elevated realized genetic load, and sharp population declines associated with invasive predators. Historical specimens exhibit higher heterozygosity and lower genetic load than contemporary samples, indicating rapid genomic erosion over the last century. Together, our results highlight introgression as a persistent force shaping Caribbean skink evolution and reveal urgent conservation risks driven by recent demographic collapse and loss of genomic resilience.

Evolutionary Journal of the Linnean Society↗

Evidence for partial overlap of male olfactory cues in lampreys

Animals rely on a mosaic of complex information to find and evaluate mates. Pheromones, often comprised of multiple components, are considered to be particularly important for species-recognition in many species. While the evolution of species-specific pheromone blends is well-described in many insects, very few vertebrate pheromones have been studied in a macro-evolutionary context. Here, we report a phylogenetic comparison of multi-component male odours that guide reproduction in lampreys. Chemical profiling of sexually mature males from eleven species of lamprey, representing six of ten genera and two of three families, indicated the chemical profiles of sexually mature male odours are partially shared among species. Behavioural assays conducted with four species sympatric in the Laurentian Great Lakes indicated asymmetric female responses to heterospecific odours, where Petromyzon marinus were attracted to male odour collected from all species tested but other species generally preferred only the odour of conspecifics. Electro-olfactogram recordings from P. marinus indicated that although P. marinus exhibited behavioural responses to odours from males of all species, at least some of the compounds that elicited olfactory responses were different in conspecific male odours compared to heterospecific male odours. We conclude that some of the compounds released by sexually mature males are shared among species and elicit olfactory and behavioural responses in P. marinus , and suggest that our results provide evidence for partial overlap of male olfactory cues among lampreys. Further characterization of the chemical identities of odour components is needed to confirm shared pheromones among species.

Journal of Experimental Biology↗

Conditions favouring Bromus tectorum dominance of endangered sagebrush steppe ecosystems

1. Ecosystem invasibility is determined by combinations of environmental variables, invader attributes, disturbance regimes, competitive abilities of resident species and evolutionary history between residents and disturbance regimes. Understanding the relative importance of each factor is critical to limiting future invasions and restoring ecosystems. 2. We investigated factors potentially controlling Bromus tectorum invasions into Artemisia tridentata ssp. wyomingensis communities across 75 sites in the Great Basin. We measured soil texture, cattle grazing intensity, gaps among perennial plants and plant cover including B. tectorum, biological soil crusts (BSCs) and bare soil. Using a priori knowledge, we developed a multivariate hypothesis of the susceptibility of Artemisia ecosystems to B. tectorum invasion and used the model to assess the relative importance of the factors driving the magnitude of such invasions. 3. Model results imply that bunchgrass community structure, abundance and composition, along with BSC cover, play important roles in controlling B. tectorum dominance. Evidence suggests abundant bunchgrasses limit invasions by limiting the size and connectivity of gaps between vegetation, and BSCs appear to limit invasions within gaps. Results also suggest that cattle grazing reduces invasion resistance by decreasing bunchgrass abundance, shifting bunchgrass composition, and thereby increasing connectivity of gaps between perennial plants while trampling further reduces resistance by reducing BSC. 4. Synthesis and applications. Grazing exacerbates Bromus tectorum dominance in one of North America's most endangered ecosystems by adversely impacting key mechanisms mediating resistance to invasion. If the goal is to conserve and restore resistance of these systems, managers should consider maintaining or restoring: (i) high bunchgrass cover and structure characterized by spatially dispersed bunchgrasses and small gaps between them; (ii) a diverse assemblage of bunchgrass species to maximize competitive interactions with B. tectorum in time and space; and (iii) biological soil crusts to limit B. tectorum establishment. Passive restoration by reducing cumulative cattle grazing may be one of the most effective means of achieving these three goals.

Journal of Applied Ecology↗

Nutritional stress affects corticosterone deposition in feathers of Caspian tern chicks

Stressful environmental conditions affect the adrenocortical function of developing animals, which can have consequences for their fitness. Discovery of the avian stress hormone corticosterone (CORT) in feathers has the potential to broaden the application of endocrine research in ecological and evolutionary studies of wild birds by providing a long-term measure of CORT secretion. Mechanisms of CORT deposition in feathers are not well known and few studies have related feather CORT to circulating plasma CORT during feather growth. Our objective was to experimentally test the validity of using feather CORT as a measure of CORT secretion in developing birds experiencing nutritional stress. Caspian tern Hydroprogne caspia chicks were fed ad libitum or restricted (35% less than ad libitum) diets for four weeks. We measured CORT in feathers from these chicks to examine the relationship between feather CORT concentrations and nutritional limitation, circulating plasma CORT, and feather development. We found that feather CORT was higher in controls fed ad libitum than in restricted individuals, despite higher levels of plasma CORT in restricted chicks compared to controls. Feather mass and growth rates were strongly and positively related to feather CORT concentrations in both treatments. This is the first experimental study to show that feather CORT concentrations can be lower in response to nutritional stress, even when plasma CORT concentrations are elevated. Our results indicate that CORT deposition in feathers may be confounded when feather mass and growth rates are compromised by nutritional stress. We conclude that feather CORT can be used for assessing nutritional stress in growing birds, but the direction of response depends on how strongly stress affects feather development.

Journal of Avian Biology↗