How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences

Arms races between avian brood parasites and their hosts often result in parasitic mimicry of host eggs, to evade rejection. Once egg mimicry has evolved, host defences could escalate in two ways: (i) hosts could improve their level of egg discrimination; and (ii) negative frequency-dependent selection could generate increased variation in egg appearance (polymorphism) among individuals. Proficiency in one defence might reduce selection on the other, while a combination of the two should enable successful rejection of parasitic eggs. We compared three highly variable host species of the Afrotropical cuckoo finch Anomalospiza imberbis, using egg rejection experiments and modelling of avian colour and pattern vision. We show that each differed in their level of polymorphism, in the visual cues they used to reject foreign eggs, and in their degree of discrimination. The most polymorphic host had the crudest discrimination, whereas the least polymorphic was most discriminating. The third species, not currently parasitized, was intermediate for both defences. A model simulating parasitic laying and host rejection behaviour based on the field experiments showed that the two host strategies result in approximately the same fitness advantage to hosts. Thus, neither strategy is superior, but rather they reflect alternative potential evolutionary trajectories.     

Interpopulation variation in reproductive traits of female masu salmon, Oncorhynchus masou

Several life history models predict that larger eggs and lower fecundity should be favored in a low-growth environment. We applied the model of Sibly et al. to seven Japanese populations of masu salmon ( Oncorhynchus masou ) in order to test the predictions that populations in which individual growth rate is low are characterized by larger eggs and lower fecundity. Two populations, Shumarinai and Shikaribetsu, had the lowest growth rates of individuals, largest egg sizes and lowest fecundities of all populations examined. In contrast, the Shiribetsu, Chitose and Uono populations had highest growth rates of individuals, smallest egg sizes and highest fecundities. The Shibetsu and Toya populations were intermediate between these two groups. The gonadsomatic index (GSI) of the Shumarinai and Shikaribetsu populations was smaller than that of all other populations. Correlation analysis indicated that populations with lower individual growth rates had larger eggs and lower fecundities. The results were consistent with the predictions of the Sibly et al. model: increased egg size which results in decreased fecundity is probably an adaptation to low-growth environments. Therefore, in masu salmon, growth differences among populations may explain interpopulation variation in egg size and fecundity.     

四川省赫坎按蚊种团蚊种卵的形态及变异

对四川赫坎按蚊种团各蚊种因个体、地区以及季节和温度的不同而产生的卵形态变异进行了观察。将中华按蚊因各种因素影响产生的变异卵,归结为“宽中曲型”、“甲断型”两类卵型,认为“宽中曲型”卵,有可能为中华按蚊正在分化过程中的类型;中华按蚊在不同季节的不同温度条件下,能够产生同“小窄甲板型”、“大窄甲板型”、“小宽甲板型”、“大宽甲板型”相似的中华按蚊卵。为了避免产生误解,建议马氏（1964、1966）所称谓的“中华按蚊类群”仍称赫坎按蚊类群为好。     

A new peculiar dinosaur egg,Sankofa pyrenaica oogen. nov. oosp. nov. from the Upper Cretaceous coastal deposits of the Aren Formation,south‐central Pyrenees,Lleida, Catalonia,Spain

Abstract: A new type of small, ovoid dinosaur egg, Sankofa pyrenaica oogen. nov. oosp. nov., with a prismatic type eggshell is described from upper Cretaceous (upper Campanian–Maastrichtian) deposits of the Montsec area, South Pyrenean Central Unit, Lleida, Catalonia, Spain. This egg type was sub‐vertically laid in only two rich monospecific sites of a single stratigraphic layer from coastal deposits of the Aren Formation, interpreted as an emerged beach ridge of a barrier island – lagoon depositional system. The size and shape of these eggs with their asymmetric poles are roughly similar to modern hen eggs, which is unusual in the Cretaceous fossil egg record. Its phylogenetic position clusters with bird and Troodontid eggs. A morphospace analysis of egg shapes shows the similarity of the new egg to a Campanian fossil bird egg from Argentina, both being intermediate between modern‐bird eggs and extinct nonavian theropod eggs. However, the eggshell microstructure of Sankofa pyrenaica differs from that of bird eggs in its incipient squamatic texture. It has a peculiar pattern of interlocking small crystals in the middle of the palisade layer, instead of the thick squamatic structure commonly present in modern avian eggshells. This new egg type is attributed to a small theropod, probably with a single oviduct like birds and whose mosaic distribution of features is a combination between that of birds and nonavian theropods. This enhances the arguments supporting the close phylogenetic relationships between both groups.     

Size variation in Brachionus plicatilis resting eggs

The effect of temperature and salinity on resting egg size of two Brachionus plicatilis (Rotifers) clones was investigated. Clones were selected according to their different behaviour in laying resting eggs: one clone ejects them, whereas they remain inside the females body in the other clone. The difference in resting eggs size between the two clones is noticeable, although the difference is not as great as that between female body size. An important temperature-salinity interaction on resting egg size has been observed. The general inverse relationship between size and temperature is only true at lower temperatures. At high temperatures size varies around the mean although could be greater than at intermediate temperatures. This is more evident at the intermediate salinity tested which is considered to be the closest to the optimum in our experiments. This pattern of variation suggests that mean size is bigger than expected, in relation to temperature and salinity, when these factors have values close to the extremes of their range, normally found in nature, and to which adaptative mechanisms can evolve. Size is bigger at the salinity — temperature low - low and high - high combinations which are the most commonly found in the temperate environments.     

Placental calcium provision in a lizard with prolonged oviductal egg retention

A prominent scenario for the evolution of viviparity and placentation in reptiles predicts a step-wise pattern with an initial phase of prolonged oviductal egg retention accompanied by progressive reduction in eggshell thickness culminating in viviparity; calcium placentotrophy evolves secondarily to viviparity. Saiphos equalis is an Australian scincid lizard with a reproductive mode that is uncommon for squamates because eggs are retained in the oviduct until late developmental stages, and the embryonic stage at oviposition varies geographically. We studied calcium mobilization by embryos in two populations with different oviductal egg retention patterns to test the hypothesis that the pattern of nutritional provision of calcium is independent of the embryonic stage at oviposition. Females from one population are viviparous and oviposit eggs containing fully formed embryos, whereas embryos in oviposited eggs of the second population are morphologically less mature, and these eggs hatch several days later. The reproductive mode of this population is denoted as prolonged oviductal egg retention. Yolk provided the highest proportion of calcium to hatchlings in both populations. Eggs of both populations were enclosed in calcified eggshells, but shells of the population with prolonged egg retention had twice the calcium content of the viviparous population and embryos recovered calcium from these eggshells. Placental transfer accounted for a substantial amount of calcium in hatchlings in both populations. Hatchling calcium concentration was higher in the population with prolonged egg retention because these embryos mobilized calcium from yolk, the eggshell and the placenta. This pattern of embryonic calcium provision in which both a calcified eggshell and placentotrophy contribute to embryonic nutrition is novel. The reproductive pattern of S. equalis illustrates that calcified eggshells are compatible with prolonged oviductal egg retention and that viviparity is not requisite to calcium placentotrophy.     

Population differences in the timing of diapause: a test of hypotheses

Summary The reproductive phenology of the freshwater copepod Diaptomus sanguineus differs markedly between populations residing in two Rhode Island ponds. In a permanent pond the population switches abruptly from making subitaneous (immediately hatching) eggs to diapausing eggs at the end of March each year. In contrast, a temporary pond population switches egg types in May, returns to production of subitaneous eggs in June, and concludes the reproductive season by making diapausing eggs in July. An ESS model suggests that the pattern of diapause expected of a copepod population is a function of annual variation in the onset of harsh conditions (catastrophe date). When variation is relatively low, the superior strategy is for diapause to begin a constant period before the mean catastrophe date. When variation is high, females should make first subitaneous eggs and then diapausing eggs irrespective of the expected catastrophe date. With discrete generations, such a population would alternate between egg types. In the permanent pond, variation of catastrophe date the spring onset of planktivory by sunfish is low, whereas in the temporary pond variation of the catastrophe (pond drying) is high. The model predicts well the phenology of the two copepod populations.In the research reported here, we tested the hypothesis that copepods from the permanent pond, which switch to diapause at the same time every year, are cued by the environment to begin diapause (i.e. by photoperiod, temperature, or both), whereas those from the temporary pond make both egg types regardless of environmental conditions. In opposition to our hypothesis, experimental results indicate that diapause in both populations is cued by the environment. The distinct reproductive phenologies documented in the two populations apparently result from the copepods responding to different environmental cues, rather than one being responsive to the environment while the other is not.     

Egg mimicry by the Pacific koel: mimicry of one host facilitates exploitation of other hosts with similar egg types

When brood parasites exploit multiple host species, egg rejection by hosts may select for the evolution of host‐specific races, where each race mimics a particular host's egg type. However, some brood parasites that exploit multiple hosts with the ability to reject foreign eggs appear to have only a single egg type. In these cases, it is unclear how the parasite egg escapes detection by its hosts. Three possible explanations are: 1) host‐specific races are present, but differences in egg morphology are difficult for the human eye to detect; 2) the brood parasite evolves a single egg type that is intermediate in appearance between the eggs of its hosts; 3) or the parasite evolves mimicry of one of its hosts, which subsequently allows it to exploit other species with similar egg morphology. Here we test these possibilities by quantifying parameters of egg appearance of the brood‐parasitic Pacific koel Eudynamys orientalis and seven of its hosts. Koel eggs laid in the nests of different hosts did not show significant differences in colour or pattern, suggesting that koels have not evolved host‐specific races. Koel eggs were similar in colour, luminance and pattern to the majority of hosts, but were significantly more similar in colour and luminance to one of the major hosts than to two other major hosts, supporting hypothesis 3. Our findings suggest that mimicry of one host can allow a brood parasite to exploit new hosts with similar egg morphologies, which could inhibit the evolution of host defences in naïve hosts.     

Egg size, composition and offspring quality in some Alcidae (Aves: Charadriiformes)

The composition of fresh and fully developed (pipping) eggs of four alcids, Razorbill, Common guillemot, Brünnich's guillemot and Atlantic puffin was examined. There were no differences in egg composition between the semi-precocial Atlantic puffin and the three species with "intermediate" developmental patterns. The absolute amount of yolk increased with egg size in fresh eggs, and the relative amount remained constant with egg size for Common guillemot and Razorbill, but decreased in the Atlantic puffin. In fully developed eggs chick weight and egg weight were closely correlated, and this was due mainly to larger eggs producing chicks with larger yolk reserves. Under some conditions chicks from larger eggs do better than those from smaller eggs. Several factors influence egg size; a comparison of first and replacement eggs laid by the same females showed that a maternal effect accounted for 60–90% of the variance in egg-size and that laying date accounted for most of the remaining variance.     

A POPULATION STUDY OF AN EQUATORIAL LAND SNAIL, LIMICOLARIA MARTENSIANA (ACHATINIDAE)

Near the equator in Uganda, the herbivorous land snail, Limicolaria martensiana , occurs in well-defined populations. These populations may be very large and the snails may in places occur at exceedingly high densities. The snails breed all the year round, but with two peaks that correspond with the two annual dry seasons. They enter dispause whenever the weather is very dry. The size of adult snails seems environmentally determined and it varies in different populations : the largest snails occur on soil rich in calcium. The shells of the snails are highly variable and polymorphic in colour and pattern. In particular, there is a streaked form that occurs in all populations, and four distinct pallid "dilute" forms. The relative frequency of the forms varies markedly in different populations. Polymorphism is greatest at high population densities and the snails are all streaked where they are rare. Polymorphism can be distinguished in Pleistocene fossil populations.     

Inoculative releases of Trichogramma ostriniae for suppression of Ostrinia nubilalis (European corn borer) in sweet corn: field biology and population dynamics

The effectiveness of inoculative releases of Trichogramma ostriniae Pang and Chen for suppression of Ostrinia nubilalis (Hübner) in sweet corn was assessed. Early-season, low-density (75,000 females ha⁻¹) releases were made, and establishment, levels of parasitism and sex ratios of emerging T. ostriniae quantified. T. ostriniae established effectively for each season that they were released, but appeared to be unable to overwinter. Parasitism levels tracked egg mass numbers closely, and T. ostriniae persisted in fields even where insecticides were applied. Parasitism by indigenous Trichogramma species was 3%. Field populations of T. ostriniae were distinctly female biased (78%), with males produced in the majority of broods. Numbers of males did not increase linearly with number of O. nubilalis eggs parasitized, but appeared to remain constant above an egg mass size of about 20 eggs. A Type-I functional response to increasing egg and egg mass density was found under field conditions, where the proportion of egg masses parasitized remained constant with increasing egg mass density. A relatively consistent percentage of eggs per egg mass was parasitized, with a linear increase in number of eggs parasitized with increasing number of eggs per egg mass. These results show that T. ostriniae established viable reproductive populations in sweet corn following inoculative release, with the potential to contribute to reduced dependence on insecticides for the control of O. nubilalis in an integrated pest management program.     

Are Cuckoos Maximizing Egg Mimicry by Selecting Host Individuals with Better Matching Egg Phenotypes?

Background

Avian brood parasites and their hosts are involved in complex offence-defense coevolutionary arms races. The most common pair of reciprocal adaptations in these systems is egg discrimination by hosts and egg mimicry by parasites. As mimicry improves, more advanced host adaptations evolve such as decreased intra- and increased interclutch variation in egg appearance to facilitate detection of parasitic eggs. As interclutch variation increases, parasites able to choose hosts matching best their own egg phenotype should be selected, but this requires that parasites know their own egg phenotype and select host nests correspondingly.

Methodology/Principal Findings

We compared egg mimicry of common cuckoo Cuculus canorus eggs in naturally parasitized marsh warbler Acrocephalus palustris nests and their nearest unparasitized conspecific neighbors having similar laying dates and nest-site characteristics. Modeling of avian vision and image analyses revealed no evidence that cuckoos parasitize nests where their eggs better match the host eggs. Cuckoo eggs were as good mimics, in terms of background and spot color, background luminance, spotting pattern and egg size, of host eggs in the nests actually exploited as those in the neighboring unparasitized nests.

Conclusions/Significance

We reviewed the evidence for brood parasites selecting better-matching host egg phenotypes from several relevant studies and argue that such selection probably cannot exist in host-parasite systems where host interclutch variation is continuous and overall low or moderate. To date there is also no evidence that parasites prefer certain egg phenotypes in systems where it should be most advantageous, i.e., when both hosts and parasites lay polymorphic eggs. Hence, the existence of an ability to select host nests to maximize mimicry by brood parasites appears unlikely, but this possibility should be further explored in cuckoo-host systems where the host has evolved discrete egg phenotypes.     

中华稻蝗五地理种群的卵滞育强度及生活史模式变异

为调查中华稻蝗Oxya chinensis的地理适应,自北纬42.3°至20.0°采集了5个地理种群的标本,比较了其子代的卵滞育发生、滞育强度及成虫虫体大小。结果表明: 不同的中华稻蝗地理种群显示了不同的光周期和温度反应模式。铁岭、济宁和泗洪种群的滞育不受光周期和温度的影响,滞育率均为100%。南方的长沙和海口种群仅部分卵进入滞育,海口种群在短日条件下的滞育率高于长日条件,卵期温度亦对其滞育有较大的影响,而长沙种群的卵滞育仅受卵期温度的调控。长沙和海口种群的卵滞育强度最弱,其次是铁岭种群,中间纬度的济宁和泗洪种群的滞育强度最高。在北方的一化性种群中,滞育强度随着纬度的降低而增强。成虫的虫体大小因栖息地纬度的变化而呈现复杂的变异,北方种群的虫体大小与栖息地纬度存在显著的负相关关系,而长沙和海口种群的虫体小于济宁和泗洪种群。结果提示中华稻蝗各种群已形成各自的地理适应机制,纬度梯度在其生活史的形成和发育中起着重要的作用。     

中国石龙子雌体繁殖特征和卵孵化的地理变异

浙江丽水和广东韶关中国石龙子均年产单窝卵,窝卵数,窝卵重和卵重均与雌体SVL呈正相关,雌体头部形态,繁殖特征,产卵起始时间和孵孵化的热依赖性等有显著的地理变异;韶关石龙子产卵起始时间为5月中旬,比丽水经子约早两周,韶关石龙子窝卵数较大,卵较小,窝卵重与丽水石龙子无显著差异。韶关石龙子特定SVL的窝卵数比丽水石龙子多2．8枚卵,中国经子卵数量和大小之间有种群间权衡,无种数内权衡,同一种群内卵数量与卵大小无关,孵化温度影响石龙子孵出幼体的一些特征,24℃孵出细幼体比32℃孵出幼体大,躯干发育好,剩余卵黄少,韶关24℃孵出幼体的体重,躯干干重小于丽水幼体,韶关32℃孵出幼体的SVL小于丽水幼体,剩余卵黄大于丽水幼体,表明适宜卵孵化温度范围有地理变异。丽水石龙子卵对极端高温和低温的耐受性较强,适宜卵孵化温度范围较宽。     

Effect of Prey and Predator Density on Predation of Rice Leaffolder Eggs by the Cricket Metioche vittaticollis

Cage experiments were conducted to quantify the predation rate of the cricket Metioche vittaticollis (Sta ˚l) on the eggs of rice leaffolder Marasmia patnalis Bradley. Egg predation by adult females was measured in response to changes in egg density, predator density and leaf area per cage. The number of eggs consumed per predator increased with egg density, without reaching a plateau. The predation rate decreased with increasing leaf area. The functional response could be adequately described with a linear Type I model, with the effect of leaf area included. This type of response to leaffolder egg density means that predation was not limited by prey handling time or satiation, but by the search rate. The search rate is here interpreted as the leaf area effectively searched for leaffolder eggs by a single predator in one day. Estimated search rates averaged 0.13 m 2 day -1 for M. vittaticollis females. The search rate of the predators increased with prey density, but a model describing a density dependent search rate explained only 3% of the total variation in search rate. Increasing predator density per cage led to a decrease in the per capita egg predation rate when predator density was more than two per m 2 leaf area. Interference might thus reduce the potential to enhance leaffolder egg predation by conservation or augmentation of predatory cricket populations.     

Genetic variation in relation to demography of peripheral pool frog populations (Rana lessonae)

Summary Genetic variation in an isolated northern metapopulation of the pool frog (Rana lessonae) in Sweden was compared to that of Central European populations using enzyme electrophoresis and literature data. Of the 31 loci scored, two (EST-2 andIDH-2) were polymorphic while no variation occurred in seven of the eight loci which are polymorphic in Central European populations.The heterozygosity level of the Swedish pool frogs is very low compared to that of other anuran populations, but their mean proportion of fertilized eggs within egg masses (97.5%) was not lower than in more heterozygous species, and their body size-specific fecundity did not differ from that of Polish conspecifics. The low genetic variability of the Swedish pool frogs is discussed in relation to features of the local populations such as size (N), calculated effective size (N _e ) reproductive success and probable history. It is concluded that long-term strong fluctuations in population size caused by reporductive failure in cold years have contributed more to the low genetic variability than could a single founder event due to a recent introduction by man.     

Role of maternal provisioning in controlling interpopulation variation in hatching size in the marine snail Nucella ostrina

This study examined the role of maternal provisioning in controlling interpopulation variation in hatching size in nine isolated populations of the intertidal gastropod Nucella ostrina, in which development to the early juvenile stage takes place within an egg capsule. Variation among populations was almost entirely due to the ratio of nurse eggs to embryo, which explained 65% of the variation in hatching size. Egg size was not a significant predictor of hatching size. Differences among seven of these populations in the nurse egg/embryo ratio were entirely due to the number of nurse eggs allocated per capsule; these populations allocated different numbers of nurse eggs per capsule but allocated the same number of embryos. Intriguingly, the two most wave-sheltered populations allocated significantly more nurse eggs and more embryos to each capsule than did the seven other populations, but they maintained nurse egg/embryo ratios consistent with patterns observed in the other populations. Inter- and intrapopulation variation in hatching size appears to be controlled largely by different mechanisms: within-population variation being controlled mainly by differences in allocation of embryos per capsule, whereas most among-population variation being due to differences in allocation of nurse eggs per capsule.     

Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism

Broad ecological shifts can render previously adaptive traits nonfunctional. It is an open question as to how and how quickly nonfunctional traits decay once the selective pressures that favored them are removed. The village weaverbird (Ploceus cucullatus) avoids brood parasitism by rejecting foreign eggs. African populations have evolved high levels of within-clutch uniformity as well as individual distinctiveness in egg color and spotting, a combination that facilitates identification of foreign eggs. In a companion study, I showed that these adaptations in egg appearance declined following introductions of weavers into habitats devoid of egg-mimicking brood parasites. Here, I use experimental parasitism in two ancestral and two introduced populations to test for changes in egg rejection behavior while controlling for changes in egg appearance. Introduced populations reject foreign eggs less frequently, but the ability of source and introduced populations to reject foreign eggs does not differ after controlling for the evolution of egg color and spotting. Therefore, egg rejection behavior in introduced populations of the village weaver has been compromised by changes in egg appearance, but there has been no significant decline in the birds' ability to recognize foreign eggs. This result reconciles earlier studies on this system and provides insights into the ways behavior can change over generations, especially in the context of recognition systems and the avoidance of brood parasitism.     

The Influence of Egg Parasitoids Belonging to the Telenomus busseolae (Hymenoptera: Scelionidae) Species Complex on Sesamia calamistis (Lepidoptera: Noctuidae) Populations in Maize Fields in Southern Benin

During the second cropping season of 1992, maize fields in southern Benin were examined twice at the pre-tasselling stage, to assess the abundance of eggs of Sesamia calamistis Hampson (Lepidoptera: Noctuidae) and egg parasitism by Telenomus busseolae Gahan (Hymenoptera: Scelionidae). They were also examined at harvest, to investigate the impact of egg parasitism early in the season on S. calamistis populations, and thus plant growth. S. calamistis eggs were found in 84.0% of the fields and on 16.8% of the plants. The parasitoid was present across the entire survey area, with the rate of egg parasitism averaging 76.4%. On average, 84.1% of the egg masses/field were parasitized, indicating that the parasitoid had a good capacity for searching. The relationship between parasitization rates and egg batch size was best described by a quadratic function, with maximum parasitism of about 95% between 1 and 25 eggs/batch. In a multiple regression analysis involving infestation levels at harvest, and soil and parasitoid variables, the T. busseolae parasitization rate was one of the major factors influencing S. calamistis densities. The yield loss due to S. calamistis decreased with increasing egg parasitism.     

Individual female common cuckoos Cuculus canorus lay constant egg types but egg appearance cannot be used to assign eggs to females

Females of the obligate brood parasitic common cuckoo Cuculus canorus are assumed to lay eggs of consistent colour and pattern and egg characteristics have been used to separate between different individuals. We tested the "constant egg-type hypothesis" in blind tests using test persons who grouped cuckoo eggs into "potential clutches" based on similarity in appearance. A correct classification of eggs laid by known (radiotagged) females supported the hypothesis. However, comparisons between maternity based on visual assessments and DNA-based parentage analyses revealed rather poor concordance between the two methods. Our findings indicate that egg characteristics cannot be used to separate between cuckoo females, even if they lay eggs with constant appearance. The reason is probably that there are only small or negligible variations in egg appearance between some females like mothers and daughters or other closely related individuals.