Terrestriality constrains salamander limb diversification: Implications for the evolution of pentadactyly

Patterns of phenotypic evolution can abruptly shift as species move between adaptive zones. Extant salamanders display three distinct life cycle strategies that range from aquatic to terrestrial (biphasic), to fully aquatic (paedomorphic) and to fully terrestrial (direct development). Life cycle variation is associated with changes in body form such as loss of digits, limb reduction or body elongation. However, the relationships among these traits and life cycle strategy remain unresolved. Here, we use a Bayesian modelling approach to test whether life cycle transitions by salamanders have influenced rates, optima and integration of primary locomotory structures (limbs and trunk). We show that paedomorphic salamanders have elevated rates of limb evolution with optima shifted towards smaller size and fewer digits compared to all other salamanders. Rate of hindlimb digit evolution is shown to decrease in a gradient as life cycles become more terrestrial. Paedomorphs have a higher correlation between hindlimb digit loss and increases in vertebral number, as well as reduced correlations between limb lengths. Our results support the idea that terrestrial plantigrade locomotion constrains limb evolution and, when lifted, leads to higher rates of trait diversification and shifts in optima and integration. The basic tetrapod body form of most salamanders and the independent losses of terrestrial life stages provide an important framework for understanding the evolutionary and developmental mechanisms behind major shifts in ecological zones as seen among early tetrapods during their transition from water to land.     

Clutch identity and predator-induced hatching affect behavior and development in a leaf-breeding treefrog

For species with complex life cycles, transitions between life stages result in niche shifts that are often associated with evolutionary trade-offs. When conditions across life stages are unpredictable, plasticity in niche shift timing may be adaptive; however, factors associated with clutch identity (e.g., genetic or maternal) may influence the effects of such plasticity. The red-eyed treefrog (Agalychnis callidryas) is an ideal organism for investigating the effects of genetics and life stage switch point timing because embryos exhibit adaptive phenotypic plasticity in hatching time. In this study, we evaluated the effects of experimentally manipulated hatching time and clutch identity on antipredator behavior of tadpoles and on developmental traits of metamorphs, including larval period, mass, SVL, and jumping ability. We found that in the presence of dragonfly nymph predator cues at 21 days post-oviposition, tadpoles reduced both their activity level and height in the water column. Furthermore, early-hatched tadpoles were less active than late-hatched tadpoles of the same age. This difference in behavior patterns of early- and late-hatched tadpoles may represent an adaptive response due to a longer period of susceptibility to odonate predators for early-hatched tadpoles, or it may be a carry-over effect mediated by early exposure to an environmental stressor (i.e., induction of early hatching). We also found that hatching time affected both behavioral traits and developmental traits, but its effect on developmental traits varied significantly among clutches. This study shows that a single early-life event may influence a suite of factors during subsequent life stages and that some of these effects appear to be dependent on clutch identity. This interaction may represent an evolutionary response to a complex life cycle and unpredictable environments, regardless of whether the clutch differences are due to additive genetic variance or maternal effects.     

Immune function in a free-living bird varies over the annual cycle, but seasonal patterns differ between years

A central hypothesis of eco-immunology proposes trade-offs between immune defences and competing physiological and behavioural processes, leading to immunological variation within and among annual-cycle stages, as has been revealed for some species. However, few studies have simultaneously investigated patterns of multiple immune indices over the entire annual cycle in free-living birds, and none has investigated the consistency of seasonal patterns across multiple years. We quantified lysis, agglutination, haptoglobin, leukocyte profiles, and body mass in free-living skylarks (Alauda arvensis) through two complete annual cycles and within and between four breeding seasons. The skylarks?? annual cycle is characterised by annually repeated changes in energy and time budgets, social structure and diet. If trade-offs relating to these cyclic changes shape evolution, predictable intra-annual immune patterns may result. Alternatively, intra-annual immune patterns may vary among years if fluctuating environmental changes affect the cost?Cbenefit balances of immune function. We found significant variation in immune indices and body mass across the annual cycle, and these patterns differed between years. Immune parameters differed between four breeding seasons, and in all years, lysis and agglutination increased as the season progressed independent of average levels. Population-level patterns (intra-annual, inter-annual, within breeding season) were consistent with within-individual patterns based on repeated measurements. We found little evidence for sex differences, and only haptoglobin was correlated (negatively) with body mass. We conclude that immune modulation is not simply a pre-programmed phenomenon that reflects predictable ecological changes. Instead, fluctuating environmental conditions that vary among years likely contribute to the immunological variation that we observed.     

Recurrent sublethal warming reduces embryonic survival,inhibits juvenile growth,and alters species distribution projections under climate change

The capacity to tolerate climate change often varies across ontogeny in organisms with complex life cycles. Recently developed species distribution models incorporate traits across life stages; however, these life‐cycle models primarily evaluate effects of lethal change. Here, we examine impacts of recurrent sublethal warming on development and survival in ecological projections of climate change. We reared lizard embryos in the laboratory under temperature cycles that simulated contemporary conditions and warming scenarios. We also artificially warmed natural nests to mimic laboratory treatments. In both cases, recurrent sublethal warming decreased embryonic survival and hatchling sizes. Incorporating survivorship results into a mechanistic species distribution model reduced annual survival by up to 24% compared to models that did not incorporate sublethal warming. Contrary to models without sublethal effects, our model suggests that modest increases in developmental temperatures influence species ranges due to effects on survivorship.     

PLEIOTROPY IN THE WILD: THE DORMANCY GENE DOG1 EXERTS CASCADING CONTROL ON LIFE CYCLES

In the wild, organismal life cycles occur within seasonal cycles, so shifts in the timing of developmental transitions can alter the seasonal environment experienced subsequently. Effects of genes that control the timing of prior developmental events can therefore be magnified in the wild because they determine seasonal conditions experienced by subsequent life stages, which can influence subsequent phenotypic expression. We examined such environmentally induced pleiotropy of developmental‐timing genes in a field experiment with Arabidopsis thaliana. When studied in the field under natural seasonal variation, an A. thaliana seed‐dormancy gene, Delay Of Germination 1 (DOG1), was found to influence not only germination, but also flowering time, overall life history, and fitness. Flowering time of the previous generation, in turn, imposed maternal effects that altered germination, the effects of DOG1 alleles, and the direction of natural selection on these alleles. Thus under natural conditions, germination genes act as flowering genes and potentially vice versa. These results illustrate how seasonal environmental variation can alter pleiotropic effects of developmental‐timing genes, such that effects of genes that regulate prior life stages ramify to influence subsequent life stages. In this case, one gene acting at the seed stage impacted the entire life cycle.     

Life cycles shape parasite evolution: comparative population genetics of salmon trematodes

Little is known about what controls effective sizes and migration rates among parasite populations. Such data are important given the medical, veterinary, and economic (e.g., fisheries) impacts of many parasites. The autogenic-allogenic hypothesis, which describes ecological patterns of parasite distribution, provided the foundation on which we studied the effects of life cycles on the distribution of genetic variation within and among parasite populations. The hypothesis states that parasites cycling only in freshwater hosts (autogenic life cycle) will be more limited in their dispersal ability among aquatic habitats than parasites cycling through freshwater and terrestrial hosts (allogenic life cycle). By extending this hypothesis to the level of intraspecific genetic variation, we examined the effects of host dispersal on parasite gene flow. Our a priori prediction was that for a given geographic range, autogenic parasites would have lower gene flow among subpopulations. We compared intraspecific mitochondrial DNA variation for three described species of trematodes that infect salmonid fishes. As predicted, autogenic species had much more highly structured populations and much lower gene flow among subpopulations than an allogenic species sampled from the same locations. In addition, a cryptic species was identified for one of the autogenic trematodes. These results show how variation in life cycles can shape parasite evolution by predisposing them to vastly different genetic structures. Thus, we propose that knowledge of parasite life cycles will help predict important evolutionary processes such as speciation, coevolution, and the spread of drug resistance.     

On nitric oxide signaling,metamorphosis, and the evolution of biphasic life cycles

Summary Complex life cycles are ancient and widely distributed, particularly so in the marine environment. Generally, the marine biphasic life cycle consists of pre‐reproductive stages that exist in the plankton for various periods of time before settling and transforming into a benthic reproductive stage. Pre‐reproductive stages are frequently phenotypically distinct from the reproductive stage, and the life cycle transition (metamorphosis) linking the larval and juvenile stages varies in extent of change but is usually rapid. Selection of suitable adult sites apparently involves the capacity to retain the larval state after metamorphic competence is reached. Thus two perennial and related questions arise: How are environmentally dependent rapid transitions between two differentiated functional life history stages regulated (a physiological issue) and how does biphasy arise (a developmental issue)? Two species of solitary ascidian, a sea urchin and a gastropod, share a nitric oxide (NO)‐dependent signaling pathway as a repressive regulator of metamorphosis. NO also regulates life history transitions among several simple eukaryotes. We review the unique properties of inhibitory NO signaling and propose that (a) NO is an ancient and widely used regulator of biphasic life histories, (b) the evolution of biphasy in the metazoa involved repression of juvenile development, (c) functional reasons why NO‐based signaling is well suited as an inhibitory regulator of metamorphosis after competence is reached, and (d) signaling pathways that regulate metamorphosis of extant marine animals may have participated in the evolution of larvae.     

Environmental context shapes immediate and cumulative costs of risk-induced early hatching

In animals with complex life cycles, fitness trade-offs across life stages determine the optimal time for transitions between stages. If these trade-offs vary predictably, adaptive plasticity in the timing of life history transitions may evolve. For instance, embryos of many species are capable of accelerating hatching to escape from egg predation and other hazards, but for plasticity in hatching timing to be selectively maintained, early hatching must also entail costs, probably in subsequent life stages. However the post-hatching environment, which influences this cost, is variable in nature. We assessed how two elements of the post-hatching environment, predator species and age structure created by hatching age plasticity, affect costs of hatching early in red-eyed treefrogs, Agalychnis callidryas. Red-eyed treefrog embryos were induced to hatch at the onset of hatching competence or near the peak of spontaneous hatching and exposed to one of three insect predators in single or mixed hatching-age treatments. Age structure created by hatching-age plasticity did not affect tadpole survivorship or growth; however, the consequences of hatching timing depended on predator species and foraging mode. Tadpoles that were induced to hatch early experienced initially higher mortality rates only with the more actively foraging predator. Nonetheless, mortality costs of accelerated hatching were apparent with all predators once we factored in the longer duration of exposure that early hatchlings experience in nature. This study suggests that extended exposure of young larvae to predators may be a general cost of early hatching, explaining why spontaneous hatching occurs later in life across variable environmental contexts.     

Among‐year variation in selection during early life stages and the genetic basis of fitness in Arabidopsis thaliana

Incomplete information regarding both selection regimes and the genetic basis of fitness limits our understanding of adaptive evolution. Among‐year variation in the genetic basis of fitness is rarely quantified, and estimates of selection are typically based on single components of fitness, thus potentially missing conflicting selection acting during other life‐history stages. Here, we examined among‐year variation in selection on a key life‐history trait and the genetic basis of fitness covering the whole life cycle in the annual plant Arabidopsis thaliana. We planted freshly matured seeds of >200 recombinant inbred lines (RILs) derived from a cross between two locally adapted populations (Italy and Sweden), and both parental genotypes at the native site of the Swedish population in three consecutive years. We quantified selection against the nonlocal Italian genotype, mapped quantitative trait loci (QTL) for fitness and its components, and quantified selection on timing of germination during different life stages. In all 3 years, the local Swedish genotype outperformed the nonlocal Italian genotype. However, both the contribution of early life stages to relative fitness, and the effects of fitness QTL varied among years. Timing of germination was under conflicting selection through seedling establishment vs. adult survival and fecundity, and both the direction and magnitude of net selection varied among years. Our results demonstrate that selection during early life stages and the genetic basis of fitness can vary markedly among years, emphasizing the need for multiyear studies considering the whole life cycle for a full understanding of natural selection and mechanisms maintaining local adaptation.     

Generation separation in simple structured life cycles: models and 48 years of field data on a tea tortrix moth

Population cycles have fascinated ecologists since the early nineteenth century, and the dynamics of insect populations have been central to understanding the intrinsic and extrinsic biological processes responsible for these cycles. We analyzed an extraordinary long-term data set (every 5 days for 48 years) of a tea tortrix moth (Adoxophyes honmai) that exhibits two dominant cycles: an annual cycle with a conspicuous pattern of four or five single-generation cycles superimposed on it. General theory offers several candidate mechanisms for generation cycles. To evaluate these, we construct and parameterize a series of temperature-dependent, stage-structured models that include intraspecific competition, parasitism, mate-finding Allee effects, and adult senescence, all in the context of a seasonal environment. By comparing the observed dynamics with predictions from the models, we find that even weak larval competition in the presence of seasonal temperature forcing predicts the two cycles accurately. None of the other mechanisms predicts the dynamics. Detailed dissection of the results shows that a short reproductive life span and differential winter mortality among stages are the additional life-cycle characteristics that permit the sustained cycles. Our general modeling approach is applicable to a wide range of organisms with temperature-dependent life histories and is likely to prove particularly useful in temperate systems where insect pest outbreaks are both density and temperature dependent.     

Coexistence of competing juvenile-adult structured populations

The Leslie-Gower model is a discrete time analog of the competition Lotka-Volterra model and is known to possess the same dynamic scenarios of that famous model. The Leslie-Gower model played a historically significant role in the history of competition theory in its application to classic laboratory experiments of two competing species of flour beetles (carried out by Park in the 1940s-1960s). While these experiments generally supported what became the Competitive Exclusion Principle, Park observed an anomalous coexistence case. Recent literature has discussed Park's 'coexistence case' by means of non-Lotka-Volterra, non-equilibrium dynamics that occur in a high dimensional model with life cycle stages. We study this dynamic possibility in the lowest possible dimension, that is to say, by means of a model involving only two species each with two life cycle stages. We do this by extending the Leslie-Gower model so as to describe the competitive interaction of two species with juvenile and adult classes. We give a complete account of the global dynamics of the resulting model and show that it allows for non-equilibrium competitive coexistence as competition coefficients are increased. We also show that this phenomenon occurs in a general class of models for competing populations structured by juvenile and adult life cycle stages.     

Identification of Risks in the Life Cycle of Nanotechnology‐Based Products

In order to realize the projected market potential of nanotechnology, the environmental, health, and safety (EHS) uncertainties posed by a nano‐product (i.e., a nanotechnology‐enabled product) need to be characterized through the identification of risks and opportunities in early stages of product development. We present a methodology to identify risks from nano‐products using a scenario analysis approach that allows for expert elicitation on a set of preidentified use and disposal scenarios and what we have labeled “risk triggers” to obtain scores on their likelihood of occurrence and severity. Use and disposal scenarios describe product life‐cycle stages that could result in risk attributed to the nano‐product, whereas risk triggers are particular to nanoparticle properties. These are potential risks, as the risk assessment community is currently debating the specific risks attributed to nanotechnology. Through such a framework, our goal is to identify which products pose greater risks, where these risks occur in the product life cycle, and the impacts of these environmental risks on society. The comparison of risk triggers across nano‐products allows relative risk ranking on axes of exposure‐ and hazard‐related risk triggers. For the specific case of air fresheners, areas of acute risks resulted from bioavailability of nanoparticles in air release and water entrainment exposure scenarios; catalytic activity of nanoparticles in inhalation and air release exposure scenarios; the harmful effects due to the antibacterial property on useful bacteria particularly in susceptible populations; and, finally, risks from the lack of nanoparticle coating stability in air release scenarios.     

THE COMPONENTS OF KIN COMPETITION

It is well known that competition among kin alters the rate and often the direction of evolution in subdivided populations. Yet much remains unclear about the ecological and demographic causes of kin competition, or what role life cycle plays in promoting or ameliorating its effects. Using the multilevel Price equation, I derive a general equation for evolution in structured populations under an arbitrary intensity of kin competition. This equation partitions the effects of selection and demography, and recovers numerous previous models as special cases. I quantify the degree of kin competition, α, which explicitly depends on life cycle. I show how life cycle and demographic assumptions can be incorporated into kin selection models via α, revealing life cycles that are more or less permissive of altruism. As an example, I give closed‐form results for Hamilton's rule in a three‐stage life cycle. Although results are sensitive to life cycle in general, I identify three demographic conditions that give life cycle invariant results. Under the infinite island model, α is a function of the scale of density regulation and dispersal rate, effectively disentangling these two phenomena. Population viscosity per se does not impede kin selection.     

Incorporating Uncertainty into a Life Cycle Assessment (LCA) Model of Short-Rotation Willow Biomass (Salix spp.) Crops

To estimate fossil fuel demand and greenhouse gas emissions associated with short-rotation willow (Salix spp.) crops in New York State, we constructed a life cycle assessment model capable of estimating point values and measures of variability for a number of key processes across eight management scenarios. The system used 445.0 to 1,052.4 MJ of fossil energy per oven-dry tonne (odt) of delivered willow biomass, resulting in a net energy balance of 18.3:1 to 43.4:1. The largest fraction of the energy demand across all scenarios was driven by the use of diesel fuels. The largest proportion of diesel fuel was associated with harvesting and delivery of willow chips seven times on 3-year rotations over the life of the crop. Similar patterns were found for greenhouse gas emissions across all scenarios, as fossil fuel use served as the biggest source of emissions in the system. Carbon sequestration in the belowground portion of the willow system provided a large carbon sink that more than compensated for carbon emissions across all scenarios, resulting in final greenhouse gas balances of ?138.4 to ?52.9 kg CO₂ eq. per odt biomass. The subsequent uncertainty analyses revealed that variability associated with data on willow yield, litterfall, and belowground biomass eliminated some of the differences between the tested scenarios. Even with the inclusion of uncertainty analysis, the willow system was still a carbon sequestration system after a single crop cycle (seven 3-year rotations) in all eight scenarios. A better understanding and quantification of factors that drive the variability in the biological portions of the system is necessary to produce more precise estimates of the emissions and energy performance of short-rotation woody crops.     

Incorporating the temporal autocorrelation of demographic rates into structured population models

Population dynamics are typically temporally autocorrelated: population sizes are positively or negatively correlated with past population sizes. Previous studies have found that positive temporal autocorrelation increases the risk of extinction due to ‘inertia’ that prolongs downward fluctuations in population size. However, temporal autocorrelation has not yet been analyzed at the level of life cycle transitions. We developed an R package, colorednoise, which creates stochastic matrix population projections with distinct temporal autocorrelation values for each matrix element. We used it to analyze long-term demographic data on 25 populations from the COMADRE and COMPADRE databases and simulate their stochastic dynamics. We found a broad range of temporal autocorrelation across species, populations and life cycle stages. The number of stage-classes in the matrix strongly affected the temporal autocorrelation of the growth rate. In the plant populations, reproduction transitions had more negative temporal autocorrelation than survival transitions, and matrices dominated by positive temporal autocorrelation had higher extinction risk, while in animal populations transition type was not associated with noise color. Our results indicate that temporal autocorrelation varies across life cycle transitions, even among populations of the same species. We present the colorednoise package for researchers to analyze the temporal autocorrelation of structured demographic rates.     

Tetrasporophytic bias coupled with heterozygote deficiency in Antarctic Plocamium sp. (Florideophyceae,Rhodophyta)

Meiosis and syngamy generate an alternation between two ploidy stages, but the timing of these two processes varies widely across taxa, thereby generating life cycle diversity. One hypothesis suggests that life cycles with long-lived haploid stages are correlated with selfing, asexual reproduction, or both. Though mostly studied in angiosperms, selfing and asexual reproduction are often associated with marginal habitats. Yet, in haploid-diploid macroalgae, these two reproductive modes have subtle but unique consequences whereby predictions from angiosperms may not apply. Along the western Antarctic Peninsula, there is a thriving macroalgal community, providing an opportunity to explore reproductive system variation in haploid-diploid macroalgae at high latitudes where endemism is common. Plocamium sp. is a widespread and abundant red macroalga observed within this ecosystem. We sampled 12 sites during the 2017 and 2018 field seasons and used 10 microsatellite loci to describe the reproductive system. Overall genotypic richness and evenness were high, suggesting sexual reproduction. Eight sites were dominated by tetrasporophytes, but there was strong heterozygote deficiency, suggesting intergametophytic selfing. We observed slight differences in the prevailing reproductive mode among sites, possibly due to local conditions (e.g., disturbance) that may contribute to site-specific variation. It remains to be determined whether high levels of selfing are characteristic of macroalgae more generally at high latitudes, due to the haploid-diploid life cycle, or both. Further investigations of algal life cycles will likely reveal the processes underlying the maintenance of sexual reproduction more broadly across eukaryotes, but more studies of natural populations are required.     

Geographic variation in life cycle strategies of a progenetic trematode

Numerous parasite species have evolved complex life cycles with multiple, subsequent hosts. In trematodes, each transmission event in multi-host life cycles selects for various adaptations, one of which is facultative life cycle abbreviation. This typically occurs through progenesis, i.e., precocious maturity and reproduction via self-fertilization within the second intermediate host. Progenesis eliminates the need for the definitive host and facilitates life cycle completion. Adopting a progenetic cycle may be a conditional strategy in response to environmental cues related to low probability of transmission to the definitive host. Here, the effects of environmental factors on the reproductive strategy of the progenetic trematode Stegodexamene anguillae were investigated using comparisons among populations. In the 3-host life cycle, S. anguillae sexually reproduces within eel definitive hosts, whereas in the progenetic life cycle, S. anguillae reproduces by selfing within the metacercaria cyst in tissues of small fish intermediate hosts. Geographic variation was found in the frequency of progenesis, independent of eel abundance. Progenesis was affected by abundance and length of the second intermediate fish host as well as encystment site within the host. The present study is the first to compare life cycle strategies among parasite populations, providing insight into the often unrecognized plasticity in parasite developmental strategies and transmission.