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1.  Potential for local adaptation in response to an anthropogenic agent of selection: effects of road deicing salts on amphibian embryonic survival and development 
Evolutionary Applications  2012;6(2):384-392.
The application of millions of tons of road deicing salts every winter in North America presents significant survival challenges to amphibians inhabiting roadside habitats. While much is known of the effects of NaCl on anuran tadpoles, less is known of effects on amphibian eggs, or any caudate life stage. In addition, little is known of the effects of MgCl2, which is now the 2nd most commonly used road deicer. Most studies have considered amphibians to be helpless victims of deicing salts, and ignore the possibility of the evolution of local adaptation to this stressor. We attempt to address these knowledge gaps and explore this evolutionary potential by examining the effects of NaCl and MgCl2 on the survival and development of eggs from different female rough-skinned newts (Taricha granulosa) from the same population. We demonstrate that both salts, at environmentally relevant concentrations, severely affect the embryonic survival and development of this amphibian, but that the effects of the salt are dependent on the identity of the mother. This female × treatment interaction results in substantial variation in tolerance to road deicing salts among newt families, providing the raw material necessary for natural selection and the evolution of local adaptation in this amphibian.
doi:10.1111/eva.12016
PMCID: PMC3586626  PMID: 23467723
amphibian; egg; local adaptation; magnesium chloride; natural selection; road deicing salt; Taricha granulosa; variation
2.  Embryonic Development and Rates of Metabolic Activity in Early and Late Hatching Eggs of the Major Malaria Vector Anopheles gambiae 
PLoS ONE  2014;9(12):e114381.
Anopheles gambiae eggs generally hatch at the completion of embryo development; two-three days post oviposition. However, staggered or delayed hatching has been observed whereby a single batch of eggs shows marked variation in time-to-hatch, with some eggs hatching 18 days post oviposition or later. The mechanism enabling delayed hatch has not been clearly elucidated but is likely mediated by environmental and genetic factors that either induce diapause or slow embryo development. This study aimed to compare metabolic activity and embryonic development between eggs collected from sub-colonies of the baseline Anopheles gambiae GAH colony previously selected for early or late time-to-hatch. Egg batches from early and late hatch sub-colonies as well as from the baseline colony were monitored for hatching. For both time-to-hatch selected sub-colonies and the baseline colony the majority of eggs hatched on day two post oviposition. Nevertheless, eggs produced by the late hatch sub-colony showed a significantly longer mean time to hatch than those produced by the early hatch sub-colony. The overall proportions that hatched were similar for all egg batches. CO2 output between eggs from early and late hatch sub-colonies showed significant differences only at 3 and 7 days post oviposition where eggs from the early hatch and the late hatch sub-colony were more metabolically active, respectively. No qualitative differences were observed in embryo development between the sub-colonies. It is concluded that all viable embryos develop to maturity at the same rate and that a small proportion then enter a state of diapause enabling them to hatch later. As it has previously been shown that it is possible to at least partially select for late hatch, this characteristic is likely to involve genetic as well as environmental factors. Delayed hatching in An. gambiae is likely an adaptation to maximise reproductive output despite the increased risk of desiccation in an unstable aquatic environment.
doi:10.1371/journal.pone.0114381
PMCID: PMC4257673  PMID: 25479444
3.  Effects of Hatching Time on Behavior and Weight Development of Chickens 
PLoS ONE  2014;9(7):e103040.
The length of the embryonic period varies both among and within species and can affect the individual phenotype in many ways, both physiologically and behaviorally. In chickens, the hatch window may last 24–48 hours (up to 10% of the incubation time), and studies have shown that incubation length may affect post-hatch growth and physiology. However, little is known about effects on behavior. We therefore investigated how behavior variation correlates with hatching time in the early life of chickens. We also measured egg weight and egg weight loss in relation to hatching time, as well as post-hatch growth. For females, there was a negative correlation between hatch time and body weight from day 4 and throughout the experiment. For males, such a correlation was only observed when testing all hatched males up until day 10. The birds were exposed to a number of behavioral tests, and a principal components analysis was performed on the variables, resulting in four components. For the largest component, termed “Passivity”, a tendency of a difference was found between early and middle male hatchers. Furthermore, a significant difference between early and middle male hatchers was found in the second component, termed “Response to novelty”. In a spatial learning test, late hatchers tended to learn slower. The behavior of females was not significantly affected by hatching time in any of these tests. This study is among the first to demonstrate a link between time of hatching and early behavior in a precocial species like the chicken, and may help shedding light on the evolutionary trade-offs between incubation length and post-hatch traits. The results may also be relevant from a perspective of stress coping and therefore also for animal welfare and productivity in the chicken industry. The mechanisms linking hatching time with post-hatch phenotype remain to be investigated.
doi:10.1371/journal.pone.0103040
PMCID: PMC4109967  PMID: 25058654
4.  Hatching Time and Alevin Growth Prior to the Onset of Exogenous Feeding in Farmed, Wild and Hybrid Norwegian Atlantic Salmon 
PLoS ONE  2014;9(12):e113697.
The onset of exogenous feeding, when juveniles emerge from the gravel, is a critical event for salmonids where early emergence and large size provide a competitive advantage in the wild. Studying 131 farmed, hybrid and wild Norwegian Atlantic salmon families, originating from four wild populations and two commercial strains, we investigated whether approximately 10 generations of selection for faster growth has also resulted in increased somatic growth prior to the onset of exogenous feeding. In addition, we tested whether relaxed selection in farms has allowed for alterations in hatching time between farmed and wild salmon. Across three cohorts, wild salmon families hatched earlier than farmed salmon families, while hybrid families displayed intermediate hatching times. While the observed differences were small, i.e., 1–15 degree-days (0–3 days, as water temperatures were c. 5–6°C), these data suggest additive genetic variation for hatching time. Alevin length prior to exogenous feeding was positively related to egg size. After removal of egg size effects, no systematic differences in alevin length were observed between the wild and farmed salmon families. While these results indicate additive genetic variation for egg development timing, and wild salmon families consistently hatched earlier than farmed salmon families, these differences were so small they are unlikely to significantly influence early life history competition of farmed and wild salmon in the natural environment. This is especially the case given that the timing of spawning among females can vary by several weeks in some rivers. The general lack of difference in size between farmed and wild alevins, strongly suggest that the documented differences in somatic growth rate between wild and farmed Norwegian Atlantic salmon under hatchery conditions are first detectable after the onset of exogenous feeding.
doi:10.1371/journal.pone.0113697
PMCID: PMC4249964  PMID: 25438050
5.  Hatching responses of subsocial spitting spiders to predation risk. 
The carrying of eggs often renders parents vulnerable to predators due to increased conspicuousness or decreased mobility. Nonetheless, egg-carrying parents can escape from the predators to which they are vulnerable. Previous studies have demonstrated heavy predation by spider-eating jumping spiders (Portia labiata) on egg-carrying spitting spider (Scytodes pallida) females, but little predation on eggless females. If the timing of hatching is phenotypically plastic, then both S. pallida females and their eggs could reduce the risk of predation by hatching early. Hence, this study examines the hatching responses of S. pallida to chemical cues from P. labiata, both in the laboratory and in the field, and addresses the following questions. (i) Do cues from predatory P. labiata influence the hatching traits of S. pallida? (ii) Are the olfactory cues from predators sufficient for predator detection by S. pallida ? (iii) Are hatching responses to predatory P. labiata controlled by egg-carrying S. pallida females, or directly by their embryos? The study provides evidence of hatching as a life-history switch point, which shows an adaptive plasticity in response to predation risk in egg-carrying S. pallida. Egg-carrying S. pallida females, but not unattended eggs, adjust egg-hatching time (the interval between oviposition and hatching) in response to the threat of predation on both the female and her eggs by P. labiata. In the presence of P. labiata, eggs that are carried by females hatch sooner; the hatchlings of these eggs are therefore smaller than hatchlings born in the absence of P. labiata. Chemical cues that are released from the draglines of P. labiata are sufficient to elicit changes in the egg-hatching traits of S. pallida. Hatching early in response to this predator may benefit both females and their offspring. To my knowledge, this is the first direct experimental study to demonstrate predator-induced hatching plasticity in spiders and, in particular, in animals with parental care.
doi:10.1098/rspb.2002.2140
PMCID: PMC1691139  PMID: 12396491
6.  Staggered larval time-to-hatch and insecticide resistance in the major malaria vector Anopheles gambiae S form 
Malaria Journal  2010;9:360.
Background
Anopheles gambiae is a major vector of malaria in the West African region. Resistance to multiple insecticides has been recorded in An. gambiae S form in the Ahafo region of Ghana. A laboratory population (GAH) established using wild material from this locality has enabled a mechanistic characterization of each resistance phenotype as well as an analysis of another adaptive characteristic - staggered larval time-to-hatch.
Methods
Individual egg batches obtained from wild caught females collected from Ghana and the Republic of the Congo were monitored for staggered larval time-to-hatch. In addition, early and late larval time-to-hatch sub-colonies were selected from GAH. These selected sub-colonies were cross-mated and their hybrid progeny were subsequently intercrossed and back-crossed to the parental strains. The insecticide susceptibilities of the GAH base colony and the time-to-hatch selected sub-colonies were quantified for four insecticide classes using insecticide bioassays. Resistance phenotypes were mechanistically characterized using insecticide-synergist bioassays and diagnostic molecular assays for known reduced target-site sensitivity mutations.
Results
Anopheles gambiae GAH showed varying levels of resistance to all insecticide classes. Metabolic detoxification and reduced target-site sensitivity mechanisms were implicated. Most wild-caught families showed staggered larval time-to-hatch. However, some families were either exclusively early hatching or late hatching. Most GAH larvae hatched early but many egg batches contained a proportion of late hatching larvae. Crosses between the time-to-hatch selected sub-colonies yielded ambiguous results that did not fit any hypothetical models based on single-locus Mendelian inheritance. There was significant variation in the expression of insecticide resistance between the time-to-hatch phenotypes.
Conclusions
An adaptive response to the presence of multiple insecticide classes necessarily involves the development of multiple resistance mechanisms whose effectiveness may be enhanced by intra-population variation in the expression of resistance phenotypes. The variation in the expression of insecticide resistance in association with selection for larval time-to-hatch may induce this kind of enhanced adaptive plasticity as a consequence of pleiotropy, whereby mosquitoes are able to complete their aquatic life stages in a variable breeding environment using staggered larval time-to-hatch, giving rise to an adult population with enhanced variation in the expression of insecticide resistance.
doi:10.1186/1475-2875-9-360
PMCID: PMC3020156  PMID: 21156042
7.  Developmental and Evolutionary History Affect Survival in Stressful Environments 
PLoS ONE  2014;9(4):e95174.
The world is increasingly impacted by a variety of stressors that have the potential to differentially influence life history stages of organisms. Organisms have evolved to cope with some stressors, while with others they have little capacity. It is thus important to understand the effects of both developmental and evolutionary history on survival in stressful environments. We present evidence of the effects of both developmental and evolutionary history on survival of a freshwater vertebrate, the rough-skinned newt (Taricha granulosa) in an osmotically stressful environment. We compared the survival of larvae in either NaCl or MgCl2 that were exposed to salinity either as larvae only or as embryos as well. Embryonic exposure to salinity led to greater mortality of newt larvae than larval exposure alone, and this reduced survival probability was strongly linked to the carry-over effect of stunted embryonic growth in salts. Larval survival was also dependent on the type of salt (NaCl or MgCl2) the larvae were exposed to, and was lowest in MgCl2, a widely-used chemical deicer that, unlike NaCl, amphibian larvae do not have an evolutionary history of regulating at high levels. Both developmental and evolutionary history are critical factors in determining survival in this stressful environment, a pattern that may have widespread implications for the survival of animals increasingly impacted by substances with which they have little evolutionary history.
doi:10.1371/journal.pone.0095174
PMCID: PMC3991610  PMID: 24748021
8.  Mother and offspring fitness in an insect with maternal care: phenotypic trade-offs between egg number, egg mass and egg care 
Background
Oviparous females have three main options to increase their reproductive success: investing into egg number, egg mass and/or egg care. Although allocating resources to either of these three components is known to shape offspring number and size, potential trade-offs among them may have key impacts on maternal and offspring fitness. Here, we tested the occurrence of phenotypic trade-offs between egg number, egg mass and maternal expenditure on egg care in the European earwig, Forficula auricularia, an insect with pre- and post-hatching forms of maternal care. In particular, we used a series of laboratory observations and experiments to investigate whether these three components non-additively influenced offspring weight and number at hatching, and whether they were associated with potential costs to females in terms of future reproduction.
Results
We found negative associations between egg number and mass as well as between egg number and maternal expenditure on egg care. However, these trade-offs could only be detected after statistically correcting for female weight at egg laying. Hatchling number was not determined by single or additive effects among the three life-history traits, but instead by pairwise interactions among them. In particular, offspring number was positively associated with the number of eggs only in clutches receiving high maternal care or consisting of heavy eggs, and negatively associated with mean egg mass in clutches receiving low care. In contrast, offspring weight was positively associated with egg mass only. Finally, maternal expenditure on egg care reduced their future reproduction, but this effect was only detected when mothers were experimentally isolated from their offspring at egg hatching.
Conclusions
Overall, our study reveals simultaneous trade-offs between the number, mass and care of eggs. It also demonstrates that these factors interact in their impact on offspring production, and that maternal expenditure on egg care possibly shapes female future reproduction. These findings emphasize that studying reproductive success requires consideration of phenotypic trade-offs between egg-number, egg mass and egg care in oviparous species.
doi:10.1186/1471-2148-14-125
PMCID: PMC4061511  PMID: 24913927
Reproduction; Parental care; Egg cannibalism; Reciprocal causation; Cost; Insect; Earwig
9.  Physiological, Behavioral and Maternal Factors That Contribute to Size Variation in Larval Amphibian Populations 
PLoS ONE  2013;8(10):e76364.
Size variance among similarly aged individuals within populations is a pattern common to many organisms that is a result of interactions between intrinsic and extrinsic traits of individuals. While genetic and maternal effects, as well as physiological and behavioral traits have been shown to contribute to size variation in animal populations, teasing apart the influence of such factors on individual growth rates remain a challenge. Furthermore, tracing the effects of these interactions across life stages and in shaping adult phenotypes also requires further exploration. In this study we investigated the relationship between genetics, hatching patterns, behaviors, neuroendocrine stress axis activity and variance in growth and metamorphosis among same-aged larval amphibians. Through parallel experiments we found that in the absence of conspecific interactions, hatch time and to a lesser extent egg clutch identity (i.e. genetics and maternal effects) influenced the propensity for growth and development in individual tadpoles and determined metamorphic traits. Within experimental groups we found that variance in growth rates was associated with size-dependent foraging behaviors and responses to food restriction. We also found an inverse relationship between glucocorticoid (GC) hormone levels and body mass and developmental stage among group-reared tadpoles, which suggests that GC expression plays a role in regulating differing within-population growth trajectories in response to density-dependent conditions. Taken together these findings suggest that factors that influence hatching conditions can have long-term effects on growth and development. These results also raise compelling questions regarding the extent to which maternal and genetic factors influence physiological and behavioral profiles in amphibians.
doi:10.1371/journal.pone.0076364
PMCID: PMC3797114  PMID: 24143188
10.  Thermal Plasticity in Life-History Traits in the Polymorphic Blue-Tailed Damselfly, Ischnura elegans: No Differences between Female Morphs 
Female polymorphism is observed in various animal species, but is particularly common in damselflies. The maintenance of this polymorphism has traditionally been explained from frequency and density dependent sexual conflict, however, the role of abiotic factors has recently attracted more interest. Here, the role of ambient temperature in shaping life-history was investigated for the three female morphs of Ischnura elegans (Vander Linden) (Zygoptera: Coenagrionidae). Eggs were obtained from the three mature female morphs for two populations in the Netherlands. Using a split-brood design, eggs of both populations were divided between a cold and a warm treatment group in the laboratory, and egg survival and hatching time were measured. Significant thermal plasticity was found in both hatching time and egg survival between both temperature treatments. However, individuals born to mothers belonging to different colour morphs did not differ in their response to temperature treatment. Independent of colour morph, clear differences in both life-history traits between the populations were found, suggesting local adaptation. Specifically, individuals from one population hatched faster but had lower egg survival in both thermal regimes. The selection force establishing fast hatching could be (facultative) bivoltinism in one of the populations compared to univoltinism in the other. This would be in line with the more southern (and more coastal) location of the presumed bivoltine population and the inverse relation between voltinism and latitude known from earlier studies. However, other natural selection forces, e.g. deterioration of the aquatic habitat, may also drive fast hatching.
doi:10.1673/031.011.11201
PMCID: PMC3281378  PMID: 22224863
adaptation; egg mortality; hatching time; phenotypic plasticity; temperature
11.  Snake and Bird Predation Drive the Repeated Convergent Evolution of Correlated Life History Traits and Phenotype in the Izu Island Scincid Lizard (Plestiodon latiscutatus) 
PLoS ONE  2014;9(3):e92233.
Predation may create strong natural selection pressure on the phenotype and life history characteristics of prey species. The Izu scincid lizards (Plestiodon latiscutatus) that inhabit the four Japanese Izu Islands with only bird predators are drab brown, mature later, lay small clutches of large eggs, and hatch large neonates. In contrast, skinks on seven islands with both snake and bird predators are conspicuously colored, mature early, lay large clutches of small eggs, and hatch small neonates. We test the hypothesis that these suites of traits have evolved independently on each island via natural selection pressures from one of two predator regimes – birds-only and birds + snakes. Using two mtDNA genes and a nuclear locus, we infer a time-calibrated phylogeny of P. latiscutatus that reveals a basal split between Mikura and all islands south, and Miyake, all islands north, and the Izu Peninsula. Populations inhabiting Miyake, Niijima, Shikine, and Toshima are not monophyletic, suggesting either multiple colonizations or an artifact of incomplete lineage sorting (ILS). We therefore developed novel phylogenetic comparative analyses that assume either a multiple colonization or more restrictive single colonization ILS scenario and found 1) statistically significant support for the of different suites of phenotypic and life history characteristics with the presence of bird-only or bird + snake predator assemblages, and 2) strong phylogenetic support for at least two independent derivations of either the “bird-only” or “snakes + birds” phenotypes regardless of colonization scenario. Finally, our time-calibrated phylogeographic analysis supports the conclusion that the ancestor to modern Izu Island P. latiscutatus dispersed from the mainland to the Izu proto-islands between 3–7.6 million years ago (Ma). These lineages remained present in the area during successive formation of the islands, with one lineage re-colonizing the mainland 0.24-0.7 Ma.
doi:10.1371/journal.pone.0092233
PMCID: PMC3965430  PMID: 24667496
12.  Hatching the Cleidoic Egg: The Role of Thyroid Hormones 
A major life stage transition in birds and other oviparous sauropsids is the hatching of the cleidoic egg. Not unlike amphibian metamorphosis, hatching in these species can be regarded as a transition from a relatively well-protected “aqueous” environment to a more hazardous and terrestrial life outside the egg, a transition in which thyroid hormones (THs) (often in concert with glucocorticoids) play an important role. In precocial birds such as the chicken, the perihatch period is characterized by peak values of THs. THs are implicated in the control of muscle development, lung maturation and the switch from chorioallantoic to pulmonary respiration, yolk sac retraction, gut development and induction of hepatic genes to accommodate the change in dietary energy source, initiation of thermoregulation, and the final stages of brain maturation as well as early post-hatch imprinting behavior. There is evidence that, at least for some of these processes, THs may have similar roles in non-avian sauropsids. In altricial birds such as passerines on the other hand, THs do not rise significantly until well after hatching and peak values coincide with the development of endothermy. It is not known how hatching-associated processes are regulated by hormones in these animals or how this developmental mode evolved from TH-dependent precocial hatching.
doi:10.3389/fendo.2013.00063
PMCID: PMC3668268  PMID: 23755041
altricial; bird; egg; embryo; hatching; precocial; reptile; thyroid hormone
13.  Egg incubation temperature differently affects female and male hatching dynamics and larval fitness in a leafhopper 
Ecology and Evolution  2012;2(4):732-739.
Temperature effects on ectotherms are widely studied particularly in insects. However, the life-history effects of temperature experienced during a window of embryonic development, that is egg stage, have rarely been considered. We simulated fluctuating temperatures and examined how this affects the operational sex ratio (OSR) of hatching as well as nymph and adult fitness in a leafhopper, Scaphoideus titanus. Specifically, after a warm or cold incubation we compared males and females hatching dynamics with their consequences on the sex ratio in the course of time, body size, weight, and developmental rate of the two populations, all reared on the same posthatching temperature. Males and females eggs respond differently, with females more sensitive to variation in incubation temperature. The different responses of both sexes have consequences on the sex ratio dynamic of hatchings with a weaker protandry after warm incubation. Temperatures experienced by eggs have more complex consequences on posthatching development. Later nymphal instars that hatched from eggs exposed to warm temperature were larger and bigger but developmental rate of the two populations was not affected. Our study demonstrates how incubation temperature could affect operational sex ratio and posthatching development in an insect and how this may be critical for population growth.
doi:10.1002/ece3.89
PMCID: PMC3399196  PMID: 22837822
Grape; insect vector; operational sex ratio; protandry; Scaphoideus titanus; sex ratio
14.  Corticosterone stimulates hatching of late-term tree lizard embryos. 
The regulation of hatching in oviparous animals is important for successful reproduction and survival, but is poorly understood. We unexpectedly found that RU-486, a progesterone and glucocorticoid antagonist, interferes with hatching of viable tree lizard (Urosaurus ornatus) embryos in a dose-dependent manner and hypothesized that embryonic glucocorticoids regulate hatching. To test this hypothesis, we treated eggs with corticosterone (CORT) or vehicle on Day 30 (85%) of incubation, left other eggs untreated, and observed relative hatch order and hatch time. In one study, the CORT egg hatched first in 9 of 11 clutches. In a second study, the CORT egg hatched first in 9 of 12 clutches, before vehicle-treated eggs in 10 of 12 clutches, and before untreated eggs in 7 of 9 clutches. On average, CORT eggs hatched 18.2h before vehicle-treated eggs and 11.6h before untreated eggs. Thus, CORT accelerates hatching of near-term embryos and RU-486 appears to block this effect. CORT may mobilize energy substrates that fuel hatching and/or accelerate lung development, and may provide a mechanism by which stressed embryos escape environmental stressors.
doi:10.1016/j.cbpa.2006.11.009
PMCID: PMC1885679  PMID: 17208477
development; glucocorticoids; oviparous; reproduction; Urosaurus ornatus; stress
15.  Understanding of the impact of chemicals on amphibians: a meta-analytic review 
Ecology and Evolution  2012;2(7):1382-1397.
Many studies have assessed the impact of different pollutants on amphibians across a variety of experimental venues (laboratory, mesocosm, and enclosure conditions). Past reviews, using vote-counting methods, have described pollution as one of the major threats faced by amphibians. However, vote-counting methods lack strong statistical power, do not permit one to determine the magnitudes of effects, and do not compare responses among predefined groups. To address these challenges, we conducted a meta-analysis of experimental studies that measured the effects of different chemical pollutants (nitrogenous and phosphorous compounds, pesticides, road deicers, heavy metals, and other wastewater contaminants) at environmentally relevant concentrations on amphibian survival, mass, time to hatching, time to metamorphosis, and frequency of abnormalities. The overall effect size of pollutant exposure was a medium decrease in amphibian survival and mass and a large increase in abnormality frequency. This translates to a 14.3% decrease in survival, a 7.5% decrease in mass, and a 535% increase in abnormality frequency across all studies. In contrast, we found no overall effect of pollutants on time to hatching and time to metamorphosis. We also found that effect sizes differed among experimental venues and among types of pollutants, but we only detected weak differences among amphibian families. These results suggest that variation in sensitivity to contaminants is generally independent of phylogeny. Some publication bias (i.e., selective reporting) was detected, but only for mass and the interaction effect size among stressors. We conclude that the overall impact of pollution on amphibians is moderately to largely negative. This implies that pollutants at environmentally relevant concentrations pose an important threat to amphibians and may play a role in their present global decline.
doi:10.1002/ece3.249
PMCID: PMC3434931  PMID: 22957147
Amphibians; ecotoxicology; meta-analysis; phylogenetic signal; publication bias; synergism
16.  The distribution of hatching time in Anopheles gambiae 
Malaria Journal  2006;5:19.
Background
Knowledge of the ecological differences between the molecular forms of Anopheles gambiae and their sibling species, An. arabiensis might lead to understanding their unique contribution to disease transmission and to better vector control as well as to understanding the evolutionary forces that have separated them.
Methods
The distributions of hatching time of eggs of wild An. gambiae and An. arabiensis females were compared in different water types. Early and late hatchers of the S molecular form were compared with respect to their total protein content, sex ratio, development success, developmental time and adult body size.
Results
Overall, the distribution of hatching time was strongly skewed to the right, with 89% of the eggs hatching during the second and third day post oviposition, 10% hatching during the next four days and the remaining 1% hatching over the subsequent week. Slight, but significant differences were found between species and between the molecular forms in all water types. Differences in hatching time distribution were also found among water types (in each species and molecular form), suggesting that the eggs change their hatching time in response to chemical factors in the water. Early hatchers were similar to late hatchers except that they developed faster and produced smaller adults than late hatchers.
Conclusion
Differences in hatching time and speed of development among eggs of the same batch may be adaptive if catastrophic events such as larval site desiccation are not rare and the site's quality is unpredictable. The egg is not passive and its hatching time depends on water factors. Differences in hatching time between species and molecular forms were slight, probably reflecting that conditions in their larval sites are rather similar.
doi:10.1186/1475-2875-5-19
PMCID: PMC1479351  PMID: 16553960
17.  Plastic Hatching Timing by Red-Eyed Treefrog Embryos Interacts with Larval Predator Identity and Sublethal Predation to Affect Prey Morphology but Not Performance 
PLoS ONE  2014;9(6):e100623.
Many animals respond to predation risk by altering their morphology, behavior, or life-history. We know a great deal about the cues prey respond to and the changes to prey that can be induced by predation risk, but less is known about how plastic responses to predators may be affected by separate plastic responses occurring earlier in life, particularly during the embryonic period. Embryos of a broad array of taxa can respond to egg- or larval-stage risks by altering hatching timing, which may alter the way organisms respond to future predators. Using the red-eyed treefrog (Agalychnis callidryas), a model for understanding the effects of plasticity across life-stages, we assessed how the combined effects of induced variation in the timing of embryo hatching and variation in the larval predator community impacted tadpole morphology, pigmentation and swimming performance. We found that A. callidryas tadpoles developed deeper tail muscles and fins and darker pigmentation in response to fish predators, either when alone or in diverse community with other predators. Tadpoles altered morphology much less so to dragonfly naiads or water bugs. Interestingly, morphological responses to predators were also affected by induced differences in hatching age, with early and late-hatched tadpoles exhibiting different allometric relationships between tail height and body length in different predator environments. Beyond induced morphological changes, fish predators often damaged tadpoles’ tails without killing them (i.e., sublethal predation), but these tadpoles swam equally quickly to those with fully intact tails. This was due to the fact that tadpoles with more damaged tails increased tail beats to achieve equal swimming speed. This study demonstrates that plastic phenotypic responses to predation risk can be influenced by a complex combination of responses to both the embryo and larval environments, but also that prey performance can be highly resilient to sublethal predation.
doi:10.1371/journal.pone.0100623
PMCID: PMC4072661  PMID: 24967896
18.  ON THE RATE OF OXYGEN CONSUMPTION BY FERTILIZED AND UNFERTILIZED EGGS  
The Journal of General Physiology  1933;16(3):497-528.
1. The rate of oxygen consumption by eggs may not merely undergo no change at fertilization, as in the case of the starfish, but it decreases to about half in Chaetopterus and in Cumingia. 2. The absolute rate of oxygen consumption in mm.3 O2 per hour per 10 mm.3 eggs differs widely in several species of unfertilized eggs. It is very low in the sea urchin, intermediary in Nereis, and high in Chaetopterus and Cumingia. The range for these eggs is approximately 0.4 to 3.1 mm.3 O2 per hour per 10 mm.3 eggs at 21°C., in the ratio of about 1:8. 3. The absolute rates of oxygen consumption by the same fertilized eggs are much more nearly the same. They lie within the range 1.3 to 2.0 mm.3 O2 per hour per 10 mm.3 eggs at 21°C., in the ratio of approximately 1:1.5. Within this same range lie the values obtained by a number of investigators using a variety of eggs of invertebrates from several phyla. Amoeba proteus and frog skin also are within this range (see Fig. 2). 4. The changes in rate of oxygen consumption at fertilization by the different species of eggs, differing both in direction and magnitude, appear to be such as to bring the rate, when development is initiated, to about the same rate, which is also the rate of other comparable normally growing cells. 5. The direction and magnitude of the change in rate at fertilization therefore appears in the cases cited to be primarily a function of the absolute rate of oxygen consumption by the unfertilized eggs, which are characterized in their peculiar inhibited condition, among other things, by a wide range of respiratory rates. 6. It is not to be supposed that this range of rates will apply at all universally to eggs, especially to eggs of extremes in proportional content of inert materials, such as large yolky eggs. Fish and amphibian eggs for example respire at a much lower rate per unit volume. The effect on surface: volume ratios attending extremes of cell size might also be expected to shift the absolute rate. 7. The absolute rate of oxygen consumption by the eggs of the alga Fucus vesiculosus is considerably higher than the rates of the animal eggs measured. It is of the same order of magnitude as the rates of several other small-celled algae, which respire at a greater rate per unit volume than most non-motile animal cells. 8. The comparatively high rates of oxygen consumption by the inhibited (unfertilized) eggs of Chaetopterus and Cumingia are not directly associated with nuclear or morphological activity of the cell since they continue at the high rate for hours after cessation of the brief initial nuclear activity, which takes place when the eggs are placed in sea water. 9. It is concluded that the rate of oxygen consumption is not necessarily and probably not generally the limiting factor which causes inhibition of the unfertilized egg. Increase in rate of oxygen consumption is not directly related to the initiation of development, in general, nor even necessarily concomitant. It is not improbable that the low rate of oxygen consumption is an immediate part of the cause of inhibition of the unfertilized sea urchin egg, but this is a special case. 10. This thesis, that the rate of oxygen consumption is not necessarily nor ordinarily the limiting factor in the inhibition of the unfertilized egg, and conversely that increase in the rate of oxygen consumption is not usually the essential feature of fertilization, is quite in agreement with the general relations between the rate of oxygen consumption on the one hand and anesthesia, growth, and development on the other in fertilized eggs and other organisms. 11. This conclusion is opposed to Loeb's explanation of the essential feature of fertilization, as an increase in oxidation rate or more strictly to generalization of his hypothesis to include eggs other than those of the sea urchins (or of other similar special cases which may be discovered). It extends to fertilization (the initiation of development) his and Wasteney's well established conclusion that "oxidation is not the independent variable in development." 12. It is suggested that the crux of the problem of fertilization lies in the nature of the inhibition of the unfertilized egg. Certain similarities between this condition, arrived at spontaneously in the case of the egg cell, and the condition of cells in narcosis or anesthesia are pointed out. 13. Although the rate of oxygen consumption by the unfertilized eggs of Chaetopterus and Cumingia cannot be regarded as the limiting factor which causes the inhibition of the eggs, in these and other cases with different absolute rates, it appears highly probable that the rate of oxygen consumption is in some way, at present obscure, tied up with or related to the condition of inhibition. This seems probable especially in view of the sharp change in rate which in most cases immediately attends cessation of the inhibition, but the relationship may be a non-causal one, as in narcosis. 14. It must be borne in mind that oxygen consumption is not necessarily a complete measure of oxidation, and that other measures such as of heat and metabolite production are necessary before the complete amount of oxidation is known. When these are completely worked out, if free energy relations are known, it is probable that more direct and inclusive relations may be found between oxidation, growth, development, and anesthesia. Generalization of Loeb's hypothesis, using "oxidation" in the broad sense might then turn out to hold, with fertilization fitting into the general scheme, but there is no basis for it at the present time.
PMCID: PMC2141218  PMID: 19872719
19.  Constant Temperature and Time Period Effects on Anopheles Gambiae Egg Hatching 
Anopheles gambiae Giles sensu stricto (Diptera: Culicidae) egg development and its relation to environmental parameters is an understudied aspect of vector biology. Although several studies have illustrated the dramatic effects of temperature on egg development, egg hatching dynamics remain unclear. The objective of this study was to expose An. gambiae eggs to various temperatures for different lengths of time and determine the impact on egg development and hatching count. Batches of mosquito eggs (n = 30 eggs/replicate) were incubated under moist conditions at temperatures of 12, 22, 27, 33, and 42°C for intervals of 1, 3, 7, and 10 days. After that, they were flooded with distilled water at 27°C, and hatching counts were observed for up to 7 days. Mosquito eggs held at 22 and 27°C had the highest overall mean hatching count. During early incubation periods, eggs held at 33°C had hatching counts comparable to 22 and 27°C, but counts decreased drastically during later incubation periods. Temperatures of 12 and 42°C reduced mosquito egg viability, because few eggs hatched in these temperature regimes. Other experiments revealed that during early embryonic development, temperature had a major effect on the developing embryo, while later in embryonic development it had no dramatic effect. Microscopic observation of the An. gambiae embryo showed that extreme low and high temperatures affected the normal development of the embryo. A regression model was developed to describe the effect of incubation temperature and incubation period on egg hatching counts, which demonstrated that the optimum temperature for egg hatching ranges from 24 to 30°C, irrespective of incubation period. The interaction between temperature and time period may have implications for dry-season survival and climate-based models of malaria risk.
PMCID: PMC2705337  PMID: 17847843
Anopheles gambiae; eggs; hatching; temperature; time period
20.  Role of Pleiotropy in the Evolution of a Cryptic Developmental Variation in Caenorhabditis elegans 
PLoS Biology  2012;10(1):e1001230.
Using vulval phenotypes in Caenorhabditis elegans, the authors show that cryptic genetic variation can evolve through selection for pleiotropic effects that alter fitness, and identify a cryptic variant that has conferred enhanced fitness on domesticated worms under laboratory conditions.
Robust biological systems are expected to accumulate cryptic genetic variation that does not affect the system output in standard conditions yet may play an evolutionary role once phenotypically expressed under a strong perturbation. Genetic variation that is cryptic relative to a robust trait may accumulate neutrally as it does not change the phenotype, yet it could also evolve under selection if it affects traits related to fitness in addition to its cryptic effect. Cryptic variation affecting the vulval intercellular signaling network was previously uncovered among wild isolates of Caenorhabditis elegans. Using a quantitative genetic approach, we identify a non-synonymous polymorphism of the previously uncharacterized nath-10 gene that affects the vulval phenotype when the system is sensitized with different mutations, but not in wild-type strains. nath-10 is an essential protein acetyltransferase gene and the homolog of human NAT10. The nath-10 polymorphism also presents non-cryptic effects on life history traits. The nath-10 allele carried by the N2 reference strain leads to a subtle increase in the egg laying rate and in the total number of sperm, a trait affecting the trade-off between fertility and minimal generation time in hermaphrodite individuals. We show that this allele appeared during early laboratory culture of N2, which allowed us to test whether it may have evolved under selection in this novel environment. The derived allele indeed strongly outcompetes the ancestral allele in laboratory conditions. In conclusion, we identified the molecular nature of a cryptic genetic variation and characterized its evolutionary history. These results show that cryptic genetic variation does not necessarily accumulate neutrally at the whole-organism level, but may evolve through selection for pleiotropic effects that alter fitness. In addition, cultivation in the laboratory has led to adaptive evolution of the reference strain N2 to the laboratory environment, which may modify other phenotypes of interest.
Author Summary
Robustness is a property of biological systems that ensures the production of reproducible phenotypes in spite of underlying environmental, stochastic, and genetic variability. A consequence of robustness is that potentially functional genetic variation is free to accumulate in natural populations because it is buffered at the phenotypic level. Even if this so-called “cryptic” genetic variation has no obvious effects under standard conditions, it may become phenotypically expressed upon major genetic or environmental perturbations. Here we used the model organism Caenorhabditis elegans to identify genetic variations involved in the cryptic evolution of vulval cell fate induction between wild strains. We found that a mutation in the essential nath-10 gene not only contributes to cryptic genetic variation in the vulval system, but also affects key life history traits that are expected to be under a strong selective pressure (brood size, age at sexual maturity, sperm number and rate of progeny production). Indeed, an allele of nath-10 that emerged during the laboratory domestication of C. elegans about 50 years ago confers a strong competitive advantage over the ancestral allele under laboratory conditions. A genetic variation that is cryptic for a robust trait can therefore affect more sensitive phenotypes and thus evolve under selection.
doi:10.1371/journal.pbio.1001230
PMCID: PMC3250502  PMID: 22235190
21.  A Meta-Analysis of Experiments Linking Incubation Conditions with Subsequent Leg Weakness in Broiler Chickens 
PLoS ONE  2014;9(7):e102682.
A series of incubation and broiler growth studies were conducted using one strain of broiler chicken (fast feathering dam line) observing incubation effects on femoral bone ash % at hatch and the ability of the bird to remain standing at 6 weeks of age (Latency-To-Lie). Egg shell temperatures during incubation were consistently recorded. Parsimonious models were developed across eight studies using stepwise multiple linear regression of egg shell temperatures over 3-day periods and both bone ash at hatch and Latency-To-Lie. A model for bone ash at hatch explained 70% of the variation in this factor and revealed an association with lower egg shell temperatures during days 4–6 and 13–15 and higher egg shell temperatures during days 16–18 of incubation. Bone ash at hatch and subsequent Latency-To-Lie were positively correlated (r = 0.57, P<0.05). A model described 66% of the variation Latency-To-Lie showing significant association of the interaction of femoral ash at hatch and lower average egg shell temperatures over the first 15 days of incubation. Lower egg shell temperature in the early to mid incubation process (days 1–15) and higher egg shell temperatures at a later stage (days 16–18) will both tend to delay the hatch time of incubating eggs. Incubation profiles that resulted in later hatching chicks produced birds which could remain standing for a longer time at 6 weeks of age. This supports a contention that the effects of incubation observed in many studies may in fact relate more to earlier hatching and longer sojourn of the hatched chick in the final stage incubator. The implication of these outcomes are that the optimum egg shell temperature during incubation for broiler leg strength development may be lower than that regarded as ideal (37.8°C) for maximum hatchability and chick growth.
doi:10.1371/journal.pone.0102682
PMCID: PMC4108365  PMID: 25054636
22.  Manipulation of Life-History Decisions Using Leptin in a Wild Passerine 
PLoS ONE  2012;7(3):e34090.
Seasonal timing of reproduction and the number of clutches produced per season are two key avian life-history traits with major fitness consequences. Female condition may play an important role in these decisions. In mammals, body condition and leptin levels are correlated. In birds, the role of leptin remains unclear. We did two experiments where we implanted female great tits with a pellet releasing leptin evenly for 14 days, to manipulate their perceived body condition, or a placebo pellet. In the first experiment where females were implanted when feeding their first brood offspring we found, surprisingly, that placebo treated females were more likely to initiate a second brood compared to leptin treated females. Only one second brood fledged two chicks while five were deserted late in the incubation stage or when the first egg hatched. No difference was found in female or male return rate or in recruitment rate of fledglings of the first brood, possibly due to the desertion of the second broods. In our study population, where there is selection for early egg laying, earlier timing of reproduction might be hampered by food availability and thus nutritional state of the female before egg laying. We therefore implanted similar leptin pellets three weeks before the expected start of egg laying in an attempt to manipulate the laying dates of first clutches. However, leptin treated females did not initiate egg laying earlier compared to placebo treated females, suggesting that other variables than the perceived body condition play a major role in the timing of reproduction. Also, leptin treatment did not affect body mass, basal metabolic rate or feeding rates in captive females. Manipulating life history decisions using experimental protocols which do not alter individuals' energy balance are crucial in understanding the trade-off between costs and benefits of life history decisions.
doi:10.1371/journal.pone.0034090
PMCID: PMC3309012  PMID: 22448288
23.  Temporal learning of predation risk by embryonic amphibians 
Biology Letters  2009;6(3):308-310.
For prey species that rely on learning to recognize their predators, natural selection should favour individuals able to learn as early as possible. The earliest point at which individuals can gather information about the identity of their potential predators is during the embryonic stage. Indeed, recent experiments have demonstrated that amphibians can learn to recognize predators prior to hatching. Here, we conditioned woodfrog embryos to recognize predatory salamander cues either in the morning or in the evening, and subsequently exposed the two-week-old tadpoles to salamander cues either in the morning or in the evening, and recorded the intensity of their antipredator behaviour. The data indicate that amphibians learn to recognize potential predators while still in the egg, and also learn the temporal component of this information, which they use later in life, to adjust the intensity of their antipredator responses throughout the day.
doi:10.1098/rsbl.2009.0798
PMCID: PMC2880039  PMID: 20007164
predator recognition; temporal learning; embryonic learning
24.  Two developmental switch points for the wing polymorphisms in the pea aphid Acyrthosiphon pisum 
EvoDevo  2013;4:30.
Background
In many insect taxa, wing polymorphism is known to be a consequence of tradeoffs between flight and other life-history traits. The pea aphid Acyrthosiphon pisum exhibits various morphs with or without wings associated with their complex life cycle including wing polyphenism in viviparous females, genetic wing polymorphism in males, and a monomorphic wingless phenotype in oviparous females and fundatrices. While wing differentiation has been investigated in some detail in viviparous females and males, these processes have not yet been elucidated in monomorphic morphs. The ontological development of the flight apparatus, including wings and flight muscles, was therefore carefully examined in oviparous females and fundatrices and compared with other morphs.
Results
The extensive histological examinations showed that flight-apparatus primordia were not at all produced throughout their postembryonic development in oviparous females and fundatrices, suggesting that during the embryonic stages the primordia are degenerated or not developed. In contrast, in viviparous females and males, the differentiation points to winged or wingless morphs occurred at the early postembryonic instars (first or second instar).
Conclusions
Based on the above observations together with previous studies, we propose that there are two developmental switch points (embryonic and postembryonic) for the flight-apparatus development in A. pisum. Since there are multiple developmental trajectories for four wingless phenotypes (wingless viviparous females, oviparous females, fandatrices, wingless males), it is suggested that the developmental pathways leading to various morphs were evolutionarily acquired independently under selective pressures specific to each morph. Especially in viviparous females, the delay of determination is thought to contribute to the condition-dependent expressions of alternative phenotypes, that is, phenotypic plasticity.
doi:10.1186/2041-9139-4-30
PMCID: PMC3843552  PMID: 24175956
Wing polymorphism; Polyphenism; Developmental pathway; Developmental switch; Primordia formation; Wing bud; Flight muscle; Embryogenesis; Postembryonic development
25.  Testing for local adaptation in brown trout using reciprocal transplants 
Background
Local adaptation can drive the divergence of populations but identification of the traits under selection remains a major challenge in evolutionary biology. Reciprocal transplant experiments are ideal tests of local adaptation, yet rarely used for higher vertebrates because of the mobility and potential invasiveness of non-native organisms. Here, we reciprocally transplanted 2500 brown trout (Salmo trutta) embryos from five populations to investigate local adaptation in early life history traits. Embryos were bred in a full-factorial design and raised in natural riverbeds until emergence. Customized egg capsules were used to simulate the natural redd environment and allowed tracking the fate of every individual until retrieval. We predicted that 1) within sites, native populations would outperform non-natives, and 2) across sites, populations would show higher performance at ‘home’ compared to ‘away’ sites.
Results
There was no evidence for local adaptation but we found large differences in survival and hatching rates between sites, indicative of considerable variation in habitat quality. Survival was generally high across all populations (55% ± 3%), but ranged from 4% to 89% between sites. Average hatching rate was 25% ± 3% across populations ranging from 0% to 62% between sites.
Conclusion
This study provides rare empirical data on variation in early life history traits in a population network of a salmonid, and large-scale breeding and transplantation experiments like ours provide powerful tests for local adaptation. Despite the recently reported genetic and morphological differences between the populations in our study area, local adaptation at the embryo level is small, non-existent, or confined to ecological conditions that our experiment could not capture.
doi:10.1186/1471-2148-12-247
PMCID: PMC3567948  PMID: 23249365
Local adaptation; Reciprocal transplants; Salmo trutta

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