Phylogenomics, Lineage Diversification Rates, and the Evolution of Diadromy in Clupeiformes (Anchovies, Herrings, Sardines, and Relatives).

Migration independently evolved numerous times in animals, with a myriad of ecological and evolutionary implications. In fishes, perhaps the most extreme form of migration is diadromy, the migration between marine and freshwater environments. Key and longstanding questions are: how many times has diadromy evolved in fishes, how frequently do diadromous clades give rise to non-diadromous species, and does diadromy influence lineage diversification rates? Many diadromous fishes have large geographic ranges with constituent populations that use isolated freshwater habitats. This may limit gene flow among some populations, increasing the likelihood of speciation in diadromous lineages relative to non-diadromous lineages. Alternatively, diadromy may reduce lineage diversification rates if migration is associated with enhanced dispersal capacity that facilitates gene flow within and between populations. Clupeiformes (herrings, sardines, shads and anchovies) is a model clade for testing hypotheses about the evolution of diadromy because it includes an exceptionally high proportion of diadromous species and several independent evolutionary origins of diadromy. However, relationships among major clupeiform lineages remain unresolved and existing phylogenies sparsely sampled diadromous species, limiting the resolution of phylogenetically-informed statistical analyses. We assembled a phylogenomic dataset and used multi-species coalescent and concatenation-based approaches to generate the most comprehensive, highly-resolved clupeiform phylogeny to date, clarifying associations among several major clades and identifying recalcitrant relationships needing further examination. We determined that variation in rates of sequence evolution (heterotachy) and base-composition (non-stationarity) had little impact on our results. Using this phylogeny, we characterized evolutionary patterns of diadromy and tested for differences in lineage diversification rates between diadromous, marine, and freshwater lineages. We identified thirteen transitions to diadromy, all during the Cenozoic Era (ten origins of anadromy, two origins of catadromy, and one origin of amphidromy), and seven losses of diadromy. Two diadromous lineages rapidly generated non-diadromous species, demonstrating that diadromy is not an evolutionary dead-end. We discovered considerably faster transition rates out of diadromy than to diadromy. The largest lineage diversification rate increase in Clupeiformes was associated with a transition to diadromy, but we uncovered little statistical support for categorically faster lineage diversification rates in diadromous versus non-diadromous fishes. We propose that diadromy may increase the potential for accelerated lineage diversification, particularly in species that migrate long distances. However, this potential may only be realized in certain biogeographic contexts, such as when diadromy allows access to ecosystems in which there is limited competition from incumbent species.

Taxonomic revision of the Pirate Perches, Aphredoderus, (Percopsiformes: Aphredoderidae) with descriptions of two new species.

Pirate Perches, Aphredoderus, are a widespread lowland freshwater fish native to the Eastern half of the United States. Aphredoderus was thought to contain a single species divided into an Eastern and Western subspecies on either side of the Appalachian Mountains with a widespread intergrade zone through much of the Eastern Gulf of Mexico and Southern Atlantic drainages. We use morphology and genetic data from specimens spanning the entire range of the genus to determine species limits within Aphredoderus. We find evidence of five species, four of which exhibit widespread sympatry in the Southeastern United States. We elevate A. sayanus sayanus and A. sayanus gibbosus to species, redescribe A. mesotrema, supplement previous descriptions, and describe two new species, A. retrodorsalis, and A. ornatus.

Intermittent Search, Not Strict Lévy Flight, Evolves under Relaxed Foraging Distribution Constraints.

AbstractThe survival of an animal depends on its success as a forager, and understanding the adaptations that result in successful foraging strategies is an enduring endeavour of behavioral ecology. Random walks are one of the primary mathematical descriptions of foraging behavior. Power law distributions are often used to model random walks, as they can characterize a wide range of behaviors, including Lévy walks. Empirical evidence indicates the prevalence and efficiency of Lévy walks as a foraging strategy, and theoretical work suggests an evolutionary origin. However, previous evolutionary models have assumed a priori that move lengths are drawn from a power law or other families of distributions. Here, we remove this restriction with a model that allows for the evolution of any distribution. Instead of Lévy walks, our model unfailingly results in the evolution of intermittent search, a random walk composed of two disjoint modes-frequent localized walks and infrequent extensive moves-that consistently outcompeted Lévy walks. We also demonstrate that foraging using intermittent search may resemble a Lévy walk because of interactions with the resources within an environment. These extrinsically generated Lévy-like walks belie an underlying behavior and may explain the prevalence of Lévy walks reported in the literature.

Riverine flow rate drives widespread convergence in the shell morphology of imperiled freshwater mussels.

Frequent and strong morphological convergence suggests that determinism tends to supersede historical contingencies in evolutionary radiations. For many lineages living within the water column of rivers and streams, hydrodynamic forces drive widespread morphological convergence. Living below the sediment-water interface may release organisms from these hydrodynamic pressures, permitting a broad array of morphologies, and thus less convergence. However, we show here that the semi-infaunal freshwater mussels have environmentally determined convergence in shell morphology. Using 3D morphometric data from 715 individuals among 164 Nearctic species, we find that species occurring in rivers with high flow rates have evolved traits that resist dislodgement from their burrowed position in the streambed: thicker shells for their body size, with the thickest sector of the shell being the most deeply buried. Species occurring in low flow environments have evolved thinner and more uniformly thickened shells, corresponding to an alternative adaptation to dislodgement: increased burrowing efficiency. Within species, individuals also show increased shell thickness for their body size at higher flow rates, suggesting that ecophenotypy may, in part, be an important mechanism for establishing populations in new environments and thus evolutionary divergence in this highly imperiledinvertebrate group.

Latitudinal trends in mating system traits in the highly self-fertilizing Lobelia inflata revealed by community science.

Mating systems in angiosperms range from obligate outcrossing to highly self-fertilizing. The belief that obligate selfing does not exist is contradicted by genetic evidence in several populations of L. inflata, in which selfing is enforced by the anthers enclosing the style. However, whether the mating systems of these populations are typical, or an extreme across the species range is unknown. Such trends are hypothesized to result from selection for reproductive assurance under mate limitation at range margins. Here, we use ~7500 iNaturalist community science images, in which stylar exsertion can be observed, to test this hypothesis in L. inflata and, for comparison, in four typical congeneric Lobelias that express a staminate, then a pistillate phase (protandry). Specifically, we analyzed the effects of latitude and range marginality on the frequency of stylar exsertion and number of exserted flowers. Outcrossing capacity in L. inflata increased at low latitudes and near the overall range center, supporting our hypothesis, with exsertion frequencies significantly lower than in congenerics. Interestingly, in outcrossing capable individuals, the number of style-exserted flowers was consistent across the species range and among species, indicating outcrossing capable L. inflata individuals resemble congenerics. These findings suggest that variation in stylar exsertion is expressed among individuals rather than by all individuals within populations. However, whether this is a result of differences in exsertion allele frequencies or of differentiation in the induction of a threshold trait requires further study. Moreover, the trends in outcrossing capability revealed here imply the potential for geographic variation in L. inflata mating system.

Bovine lead exposure from informal battery recycling in India.

We provide an estimate of annual bovine lead exposure and attributable mortality at informal lead acid battery recycling sites in India. We use Pure Earth's Toxic Sites Identification Program database, the FAO's Gridded Livestock dataset, and a Poisson plume model of lead particle air dispersion to estimate site-level mortality. We calculate that India suffers 2370 excess bovine fatalities each year, resulting in more than USD $2.1 million of economic damage. The distribution of damages by location is highly skewed. While we find most sites (86.3%) induce no mortalities, 6.2% of sites induce minor damage (1 to 5 fatalities), 4.1% induce moderate damage (6 to 20 fatalities), and 3.4% induce severe damage (21 + fatalities). These findings highlight the importance of geospatial data to prioritize mitigation efforts and identify a previously unquantified burden on the rural poor.

Promoting blood donation through social media: Evidence from Brazil, India and the USA.

Social media has the potential to encourage prosocial behaviors at scale, yet very little causal evidence exists on the impact of related efforts. Blood donation is a particularly difficult, but essential prosocial behavior that is often critically undersupplied. We examine the effect of Facebook's blood donation tool on voluntary blood donation. We partnered with four major blood banks in the United States covering 363 collection facilities in 46 states and Washington, D.C. We tracked the tool's impact on blood donations during its staggered rollout on a sample of more than 47,000 facility-date observations from March 2019 to September 2019. The tool caused an increase of 0.55 total donations per facility per day (+4.0% [95% CI: 0.04%-8.0%]), and an increase of 0.15 donations from first-time donors per facility per day (+18.9% [95% CI: 4.7%-33.1%]). Longitudinal evidence from Brazil and India suggests the share of donors who both received a message from the tool and stated they were influenced by Facebook to donate increased from 0% to 14.1% [95% CI: 12.1%-16.2%] in the first year of the tool's deployment (i.e., September 2018 to August 2019). These meaningful increases, especially from first-time donors, demonstrate that social media platforms can play an important role in fostering offline prosocial behaviors that benefit the health and well-being of societies around the world.

The evolutionary maintenance of Lévy flight foraging.

Lévy flight is a type of random walk that characterizes the behaviour of many natural phenomena studied across a multiplicity of academic disciplines; within biology specifically, the behaviour of fish, birds, insects, mollusks, bacteria, plants, slime molds, t-cells, and human populations. The Lévy flight foraging hypothesis states that because Lévy flights can maximize an organism's search efficiency, natural selection should result in Lévy-like behaviour. Empirical and theoretical research has provided ample evidence of Lévy walks in both extinct and extant species, and its efficiency across models with a diversity of resource distributions. However, no model has addressed the maintenance of Lévy flight foraging through evolutionary processes, and existing models lack ecological breadth. We use numerical simulations, including lineage-based models of evolution with a distribution of move lengths as a variable and heritable trait, to test the Lévy flight foraging hypothesis. We include biological and ecological contexts such as population size, searching costs, lifespan, resource distribution, speed, and consider both energy accumulated at the end of a lifespan and averaged over a lifespan. We demonstrate that selection often results in Lévy-like behaviour, although conditional; smaller populations, longer searches, and low searching costs increase the fitness of Lévy-like behaviour relative to Brownian behaviour. Interestingly, our results also evidence a bet-hedging strategy; Lévy-like behaviour reduces fitness variance, thus maximizing geometric mean fitness over multiple generations.

Tooth replacement and attachment morphology in the Pacific Leaping Blenny, Alticus arnoldorum (Blenniiformes: Blenniidae: Salariini) with a discussion on tooth function.

Modes of teleost tooth replacement and attachment have historically been described using discrete classification systems that categorize major patterns across taxa. While useful, these discrete classification schemes understate teleost tooth diversity. The "unattached" dentition of salariin combtooth blennies (Blenniiformes: Blenniidae: Salariini) is frequently overlooked due to its perceived complexity, so we examined the Pacific Leaping Blenny, Alticus arnoldorum, to describe this complex morphology. Using a range of methods including histology, SEM, microCT scanning, and clearing and staining, we establish a descriptive model of tooth replacement for A. arnoldorum. We then use our descriptive model of tooth replacement to propose a hypothesis of tooth function in salariin blennies. Our results show that A. arnoldorum exhibits grouped, extraosseous replacement of feeding teeth upon a discontinuous, permanent dental lamina. We also find that tooth replacement occurs within lip tissue that is laterally displaced from the distal margins of the jaw bones, a process previously undocumented in teleost fish. Feeding teeth attach to the dentigerous bone via a primary attachment mode consisting of a continuous collagen band at the posterior base of the teeth, and a secondary attachment mode consisting of epithelial cells. Alticus arnoldorum presents novel modes of tooth replacement and attachment that challenge historical classification modes of teleost dentition. Our descriptive tooth replacement model also provides a reliable framework to propose hypotheses of tooth function that can be applied in future comparative studies on salariin blennies and other long-toothed teleosts to further elucidate the functional role of long-toothed fishes in aquatic ecosystems.

Profitability of climate-smart soil fertility investment varies widely across sub-Saharan Africa.

Soil fertility investments in sub-Saharan Africa, where budgetary resources are scarce, must be well targeted. Using a causal forest algorithm and an experimental maize trial dataset matched with geocoded rainfall, temperature and soils data, we modelled site-specific, ex ante distributions of yield response and economic returns to fertilizer use. Yield response to fertilizer use was found to vary with growing season temperature and precipitation and soil conditions. Fertilizer use profitability-defined as clearing a 30% internal rate of return in at least 70% of the years-was robust to growing season climate and the fertilizer-to-maize price ratio in several locations but not in roughly a quarter of the analysed area. The resulting profitability-assessment tool can support decision makers when climate conditions at planting are unknown and sheds light on the profitability determinants of different regions, which is key for effective smallholder farm productivity-enhancing strategies.

Patterns of Body Shape Diversity and Evolution in Intertidal and Subtidal Lineages of Combtooth Blennies (Blenniidae).

Marine intertidal zones can be harsher and more dynamic than bordering subtidal zones, with extreme and temporally variable turbulence, water velocity, salinity, temperature, and dissolved oxygen levels. Contrasting environmental conditions and ecological opportunities in subtidal versus intertidal habitats may generate differing patterns of morphological diversity. In this study we used phylogenetic comparative methods, measurements of body length, and two-dimensional landmarks to characterize body shape and size diversity in combtooth blennies (Ovalentaria: Blenniidae) and test for differences in morphological diversity between intertidal, subtidal, and supralittoral zones. We found that subtidal combtooth blennies have significantly higher body shape disparity and occupy a region of morphospace three times larger than intertidal lineages. The intertidal morphospace was almost entirely contained within the subtidal morphospace, showing that intertidal combtooth blennies did not evolve unique body shapes. We found no significant differences in body size disparity between tidal zones, no correlations between body shape and tidal zone or body size and tidal zone, and no body shape convergence associated with tidal zone. Our findings suggest that a subset of combtooth blenny body shapes are suitable for life in both subtidal and intertidal habitats. Many species in regions of morphospace unique to subtidal combtooth blennies exhibit distinct microhabitat use, which suggests subtidal environments promoted morphological diversification via evolutionary microhabitat transitions. In contrast, limited intertidal body shape diversity may be due to strong selective pressures that constrained body shape evolution and environmental filtering that prevented colonization of intertidal zones by certain subtidal body shapes.

Latitudinal variation in norms of reaction of phenology in the greater duckweed Spirodela polyrhiza.

Variable environments may result in the evolution of adaptive phenotypic plasticity when cues reliably indicate an appropriate phenotype-environment match. Although adaptive plasticity is well established for phenological traits expressed across environments, local differentiation in norms of reaction is less well studied. The switch from the production of regular fronds to overwintering 'turions' in the greater duckweed Spirodela polyrhiza is vital to fitness and is expressed as a norm of reaction induced by falling temperatures associated with the onset of winter. However, the optimal norm of reaction to temperature is expected to differ across latitudes. Here, we test the hypothesis that a gradient in the length and predictability of growing seasons across latitudes results in the evolution of reaction norms characterized by earlier turion production at higher latitudes. We test this by collecting S. polyrhiza from replicate populations across seven latitudes from Ontario to Florida and then assessing differentiation in thermal reaction norms of turion production along a common temperature gradient. As predicted, northern populations produce turions at a lower birth order and earlier; a significant latitude-by-temperature interaction suggests that reaction norm differentiation has occurred. Our results provide evidence of differentiation in reaction norms across latitudes in a phenological trait, and we discuss how the adaptive significance of this plasticity might be further tested.

Delusions of grandeur: Seed count is not a good fitness proxy under individual variation in phenology.

The concept of fitness is central to evolutionary biology, yet it is difficult to define and to measure. In plant biology, fitness is often measured as seed count. However, under an array of circumstances, seed count may be a biased proxy of fitness, for example when individuals vary in allocation to sexual versus asexual reproduction. A more subtle example, but also likely to be important in natural populations, is when interindividual variation in conditions during development results in variation in offspring quality among seed parents. In monocarpic (semelparous) plants, this is expected to result from variation in effective season length experienced among individuals that reach reproductive maturity at different times. Here, we manipulate growing season length to ask whether seed count is an accurate representation of parental fitness in the monocarpic herb Lobelia inflata. Simple seed count suggests a paradoxical fitness advantage under constrained-season length. However, we find that the apparent fitness advantage of a constrained-season length is overridden by low relative per-seed fitness. Furthermore, the fitness deficit in the constrained environment is associated primarily with an accelerating decrease in viability and seedling survival in seeds derived from fruits produced progressively later in the season. In this study, the overall fitness value of a seed under a constrained season is 0.774 of that observed under a long season.

Genotype-environment interaction and the maintenance of genetic variation: an empirical study of Lobelia inflata (Campanulaceae).

High levels of genetic variation are often observed in natural populations, suggesting the action of processes such as frequency-dependent selection, heterozygote advantage and variable selection. However, the maintenance of genetic variation in fitness-related traits remains incompletely explained. The extent of genetic variation in obligately self-fertilizing populations of Lobelia inflata (Campanulaceae L.) strongly implies balancing selection. Lobelia inflata thus offers an exceptional opportunity for an empirical test of genotype-environment interaction (G × E) as a variance-maintaining mechanism under fluctuating selection: L. inflata is monocarpic and reproduces only by seed, facilitating assessment of lifetime fitness; genome-wide homozygosity precludes some mechanisms of balancing selection, and microsatellites are, in effect, genotypic lineage markers. Here, we find support for the temporal G × E hypothesis using a manipulated space-for-time approach across four environments: a field environment, an outdoor experimental plot and two differing growth-chamber environments. High genetic variance was confirmed: 83 field-collected individuals consisted of 45 distinct microsatellite lineages with, on average, 4.5 alleles per locus. Rank-order fitness, measured as lifetime fruit production in 16 replicated multilocus genotypes, changed significantly across environments. Phenotypic differences among microsatellite lineages were detected. Results thus support the G × E hypothesis in principle. However, the evaluation of the effect size of this mechanism and fitness effects of life-history traits will require a long-term study of fluctuating selection on labelled genotypes in the field.

Understanding Maladaptation by Uniting Ecological and Evolutionary Perspectives.

Evolutionary biologists have long trained their sights on adaptation, focusing on the power of natural selection to produce relative fitness advantages while often ignoring changes in absolute fitness. Ecologists generally have taken a different tack, focusing on changes in abundance and ranges that reflect absolute fitness while often ignoring relative fitness. Uniting these perspectives, we articulate various causes of relative and absolute maladaptation and review numerous examples of their occurrence. This review indicates that maladaptation is reasonably common from both perspectives, yet often in contrasting ways. That is, maladaptation can appear strong from a relative fitness perspective, yet populations can be growing in abundance. Conversely, resident individuals can appear locally adapted (relative to nonresident individuals) yet be declining in abundance. Understanding and interpreting these disconnects between relative and absolute maladaptation, as well as the cases of agreement, is increasingly critical in the face of accelerating human-mediated environmental change. We therefore present a framework for studying maladaptation, focusing in particular on the relationship between absolute and relative fitness, thereby drawing together evolutionary and ecological perspectives. The unification of these ecological and evolutionary perspectives has the potential to bring together previously disjunct research areas while addressing key conceptual issues and specific practical problems.

Causes of maladaptation.

Evolutionary biologists tend to approach the study of the natural world within a framework of adaptation, inspired perhaps by the power of natural selection to produce fitness advantages that drive population persistence and biological diversity. In contrast, evolution has rarely been studied through the lens of adaptation's complement, maladaptation. This contrast is surprising because maladaptation is a prevalent feature of evolution: population trait values are rarely distributed optimally; local populations often have lower fitness than imported ones; populations decline; and local and global extinctions are common. Yet we lack a general framework for understanding maladaptation; for instance in terms of distribution, severity, and dynamics. Similar uncertainties apply to the causes of maladaptation. We suggest that incorporating maladaptation-based perspectives into evolutionary biology would facilitate better understanding of the natural world. Approaches within a maladaptation framework might be especially profitable in applied evolution contexts - where reductions in fitness are common. Toward advancing a more balanced study of evolution, here we present a conceptual framework describing causes of maladaptation. As the introductory article for a Special Feature on maladaptation, we also summarize the studies in this Issue, highlighting the causes of maladaptation in each study. We hope that our framework and the papers in this Special Issue will help catalyze the study of maladaptation in applied evolution, supporting greater understanding of evolutionary dynamics in our rapidly changing world.

Molecules and morphology reveal 'new' widespread North American freshwater mussel species (Bivalvia: Unionidae).

In the Family Unionidae, the greatest radiation of freshwater mussels, malacologists have been misled by extreme intraspecific shell variation and conversely interspecific conchological stasis or convergence. We characterized the genetic and morphological diversity of two phenotypes of Lampsilis teres from specimens (n = 108) collected across its distribution using geometric and traditional morphometrics and multilocus molecular phylogenetics to test the hypothesis that phenotypes represent separate species. Results from our morphometric and molecular phylogenetic analyses unanimously indicate that L. teres sensu lato is made up of two divergent, widespread species with overlapping distributions. We describe a new species and provide a revised description of L. teres sensu stricto. We use morphometrics and machine-learning classification algorithms to test if shell morphology alone can be used to discriminate between these species. Classification percentages of 97.02% and 93.86% demonstrate that shell morphology is highly informative for species identification. This study highlights our lack of understanding of species diversity of freshwater mussels and the importance of multiple characters and quantitative approaches to species delimitation.

Sensor data to measure Hawthorne effects in cookstove evaluation.

This data in brief article includes estimated time cooking based on temperature sensor data taken every 30 min from three stone fires and introduced fuel-efficient Envirofit stoves in approximately 168 households in rural Uganda. These households were part of an impact evaluation study spanning about six months to understand the effects of fuel-efficient cookstoves on fuel use and pollution. Daily particulate matter (pollution) and fuelwood use data are also included. This data in brief file only includes the weeks prior to, during, and after an in-person measurement team visited each home. The data is used to analyze whether households change cooking patterns when in-person measurement teams are present versus when only the temperature sensor is in the home.

Systematics of the combtooth blenny clade Omobranchus (Blenniidae: Omobranchini), with notes on early life history stages.

The combtooth blenny (Blenniidae) genus Omobranchus contains small, cryptobenthic fishes common to nearshore habitats throughout the Indo-West Pacific. Recent molecular systematic studies have resolved Omobranchus as monophyletic but little research has been done to resolve species-level relationships. Herein, phylogenetic analyses of one mitochondrial (CO1) and four nuclear (ENC1, myh6, sreb2, and tbr1) genes provide evidence for the monophyly of Omobranchus and support for the elongatus and banditus species group. Sampling of multiple individuals from widespread species (O. ferox, O. punctatus, and O. elongatus) suggested that the Thai-Malay Peninsula is a phylogeographic break that may be a historic barrier to gene flow. Additionally, common meristics and other morphological characters are used to describe an early life history stage of O. ferox and O. punctatus.

Phylogenetic analysis of trophic niche evolution reveals a latitudinal herbivory gradient in Clupeoidei (herrings, anchovies, and allies).

Biotic and abiotic forces govern the evolution of trophic niches, which profoundly impact ecological and evolutionary processes and aspects of species biology. Herbivory is a particularly interesting trophic niche because there are theorized trade-offs associated with diets comprised of low quality food that might prevent the evolution of herbivory in certain environments. Herbivory has also been identified as a potential evolutionary "dead-end" that hinders subsequent trophic diversification. For this study we investigated trophic niche evolution in Clupeoidei (anchovies, sardines, herrings, and their relatives) and tested the hypotheses that herbivory is negatively correlated with salinity and latitude using a novel, time-calibrated molecular phylogeny, trophic guilds delimited using diet data and cluster analysis, and standard and phylogenetically-informed statistical methods. We identified eight clupeoid trophic guilds: molluscivore, terrestrial invertivore, phytoplanktivore, macroalgivore, detritivore, piscivore, crustacivore, and zooplanktivore. Standard statistical methods found a significant negative correlation between latitude and the proportion of herbivorous clupeoids (herbivorous clupeoid species/total clupeoid species), but no significant difference in the proportion of herbivorous clupeoids between freshwater and marine environments. Phylogenetic least squares regression did not identify significant negative correlations between latitude and herbivory or salinity and herbivory. In clupeoids there were five evolutionary transitions from non-herbivore to herbivore guilds and no transitions from herbivore to non-herbivore guilds. There were no transitions to zooplanktivore, the most common guild, but it gave rise to all trophic guilds, except algivore, at least once. Transitions to herbivory comprised a significantly greater proportion of diet transitions in tropical and subtropical (<35°) relative to temperate areas (>35°). Our findings suggest cold temperatures may constrain the evolution of herbivory and that herbivory might act as an evolutionary "dead-end" that hinders subsequent trophic diversification, while zooplanktivory acts as an evolutionary "cradle" that facilitates trophic diversification.