Obligate brood parasites as selective agents for evolution of egg appearance in passerine birds

Many passerine host species have counteracted the parasite egg mimicry in their coevolutionary arms race with the common cuckoo (Cuculus canorus) by evolving increased interclutch and reduced intraclutch variation in egg appearance. Such variations make it easier for hosts to recognize a foreign egg, reduce the possibility of making recognition errors, and reduce the ability of the cuckoo to mimic the eggs of a particular host. Here, we investigate if such clutch characteristics have evolved among North American passerines. We predict that due to the absence of brood parasites with egg mimicry on this continent, these passerines should (1) not show any relationship between rejection rates and intra- or interclutch variation, and (2) intraclutch variation should be lower and interclutch variation higher in European hosts exposed to cuckoo parasitism as compared to North American hosts parasitized by cowbirds. Here we present data that show support for most of these and other predictions, as well as when controlling statistically for effects of common descent. However, the effect of continent on intraclutch variation was less than predicted and we discuss a possible reason for this. All things considered, the results demonstrate that parasitism by a specialist brood parasite with egg mimicry is a powerful selective force regarding the evolution of egg characteristics in passerine birds.     

The importance of clutch characteristics and learning for antiparasite adaptations in hosts of avian brood parasites

There is considerable variation in rejection rates of parasitic eggs among hosts of avian brood parasites. In this article, we develop a model that can be used to predict host egg rejection behavior in brood parasite-host systems in general, by considering both intra- and interclutch variation in host egg appearance; clutch characteristics that may be important in calculating the fitness of individuals adopting rejecter or acceptor strategies. In addition, we consider the importance of learning the appearance of own eggs during the first breeding attempt and host probability of survival between breeding seasons on evolution of rejection behavior. Based on this model we can predict at which level of parasitism fitness of rejecter individuals is higher than that of acceptor individuals and vice versa. The model analyses show that variation in egg appearance can be a key factor for the evolution of host defense against parasitism. In more detail, analyses show that we should expect to find a prolonged learning period only in hosts that have a high intraclutch variation in egg appearance, because such hosts may potentially experience high costs in terms of recognition errors. Furthermore, learning is in general more adaptive in parasite-host systems in which hosts do have some reproductive success even when parasitized, and when parasitism rates are moderate. By including variables that have not been considered in previous models, our model represents a useful tool in investigations of host rejection behavior in various host-parasite systems.     

Egg color variation,but not egg rejection behavior,changes in a cuckoo host breeding in the absence of brood parasitism

Interactions between parasitic cuckoos and their songbird hosts form a classical reciprocal “arms race,” and are an excellent model for understanding the process of coevolution. Changes in host egg coloration via the evolution of interclutch variation in egg color or intraclutch consistency in egg color are hypothesized counter adaptations that facilitate egg recognition and thus limit brood parasitism. Whether these antiparasitism strategies are maintained when the selective pressure of parasitism is relaxed remains debated. However, introduced species provide unique opportunities for testing the direction and extent of natural selection on phenotypic trait maintenance and variation. Here, we investigated egg rejection behavior and egg color polymorphism in the red‐billed leiothrix (Leiothrix lutea), a common cuckoo (Cuculus canorus) host, in a population introduced to Hawaii 100 years ago (breeding without cuckoos) and a native population in China (breeding with cuckoos). We found that egg rejection ability was equally strong in both the native and the introduced populations, but levels of interclutch variation and intraclutch consistency in egg color in the native population were higher than in the introduced population. This suggests that egg rejection behavior in hosts can be maintained in the absence of brood parasitism and that egg appearance is maintained by natural selection as a counter adaptation to brood parasitism. This study provides rare evidence that host antiparasitism strategies can change under parasite‐relaxed conditions and reduced selection pressure.     

Rejection of parasitic eggs in relation to egg appearance in magpies

The coevolutionary process between avian brood parasites and their hosts predicts that low intraclutch variation in egg colour appearance favours egg discrimination of parasite eggs by hosts. Low intraclutch variation would also result in high interclutch variation, which would increase the difficulty of evolution of mimicry by the cuckoo, because many host colour patterns might coexist in the same host population. We explored this possibility using an experimental approach in the common magpie, Pica pica, and great spotted cuckoo, Clamator glandarius, system. We artificially parasitized magpie nests with great spotted cuckoo model eggs to assess host response in two populations in Spain (Guadix and Doñana) in relation to intraclutch variation in egg appearance, measured by ultraviolet-visible reflectance spectrophotometry. Individuals that rejected model cuckoo eggs had higher intraclutch variation than accepters, suggesting that an increase, rather than a decrease, in intraclutch variation in magpie egg appearance was advantageous for cuckoo egg discrimination.     

Nest Sanitation as the Evolutionary Background for Egg Ejection Behaviour and the Role of Motivation for Object Removal

Higher interclutch colour variation can evolve under the pressure of brood parasitism to increase the detection of parasitic eggs. Nest sanitation could be a prerequisite for the evolution of anti-parasite defence in terms of egg ejection. In this respect, we used nest sanitation behaviour as a tool to identify: i) motivation and its underlying function and, ii) which features provoke ejection behaviour. Therefore, we experimentally tested whether size, colour or shape may influence ejection behaviour using artificial flat objects. We found a high interclutch variation in egg colouration and egg size in our tree sparrow (Passer montanus) population. Using colour and size we were in fact able to predict clutch affiliation for each egg. Our experiments further revealed the existence of direct anti-parasite behaviours and birds are able to recognise conspecific eggs, since only experimentally-deposited eggs have been removed. Moreover, experiments with different objects revealed that the motivation of tree sparrows to remove experimental objects from their nests was highest during egg laying for objects of varying size, most likely because of parasitism risk at this breeding stage. In contrary, motivation to remove white objects and objects with edges was higher during incubation stage as behavioural patterns connected to hatching started to emerge. The fact that rejection rate of our flat objects was higher than real egg ejection, suggests that egg ejection in tree sparrows and probably more general in small passerines, to be limited by elevated costs to eject eggs with their beaks. The presence of anti-parasite behaviour supports our suggestion that brood parasitism causes variation in egg features, as we have found that tree sparrows can recognise and reject conspecific eggs in their clutch. In conclusion, in tree sparrows it seems that nest sanitation plays a key role in the evolution of the removal of parasitic eggs.     

Egg rejection and clutch phenotype variation in the plain prinia Prinia inornata

Avian hosts of brood parasites can evolve anti‐parasitic defenses to recognize and reject foreign eggs from their nests. Theory predicts that higher inter‐clutch and lower intra‐clutch variation in egg appearance facilitates hosts to detect parasitic eggs as egg‐rejection mainly depends on the appearance of the egg. Therefore, we predict that egg patterns and rejection rates will differ when hosts face different intensity of cuckoo parasitism. We tested this prediction in two populations of the plain prinia Prinia inornata: Guangxi in mainland China with high diversity and density of cuckoo species, and Taiwan where there is only one breeding cuckoo species, the oriental cuckoo Cuculus optatus. As expected, egg patterns were similar within clutches but different among clutches (polymorphic eggs) in the mainland population, while the island population produced more uniform egg morphs. Furthermore, the mainland population showed a high rate of egg rejection, while the island population exhibited dramatically reduced egg grasp‐rejection ability in the absence of parasitism by the common cuckoo Cuculus canorus. Our study suggests that prinias show lower intra‐clutch consistency in egg colour and lose egg‐rejecting ability under relaxed selection pressure from brood parasitism.     

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.     

Timing of current reproduction directly affects future reproductive output in European coots

Life-history theory suggests that the variation in the seasonal timing of reproduction within populations may be explained on the basis of individual optimization. Optimal breeding times would vary between individuals as a result of trade-offs between fitness components. The existence of such trade-offs has seldom been tested empirically. We experimentally investigated the consequences of altered timing of current reproduction for future reproductive output in the European coot (Fulica atra). First clutches of different laying date were cross-fostered between nests, and parents thereby experienced a delay or an advance in the hatching date. The probability and success of a second brood, adult survival until and reproduction in the next season were then compared to the natural variation among control pairs. Among control pairs the probability of a second brood declined with the progress of season. Delayed pairs were less likely and advanced pairs were more likely to produce a second brood. These changes were quantitatively as predicted from the natural seasonal decline. The number of eggs in the second clutch was positively related to egg number in the first clutch and negatively related to laying date. Compared to the natural variation, delayed females had more and advanced females had fewer eggs in their second clutch. The size of the second brood declined with season, but there was no significant effect of delay or advance. Local adult survival was higher following a delay and reduced following an advance. The effect of the experiment on adult survival was independent of sex. Laying date and clutch size of females breeding in the next year were not affected by treatment. The study demonstrates the existence of a trade-off between increased probability of a second brood and decreased parental survival for early breeding. Timing-dependent effects of current reproduction on future reproductive output may thus play an important role in the evolution of the seasonal timing of reproduction.     

Evolution of variation in egg color and marking pattern in European passerines: adaptations in a coevolutionary arms race with the cuckoo, Cuculus canorus

In a coevolutionary arms race between the cuckoo (Cuculus canorus)and its host species, both sides should evolve adaptations thatwill ensure the survival of their own offspring. The appearanceof the eggs is central in this race. We investigated the occurrenceof a defense mechanism that has not previously been demonstrated:the evolution of an increase in the variation in egg appearance(color and markings) between clutches, and an increase in theuniformity of eggs within clutches. We quantified the degreeof homogeneity within and between clutches in the color andmarking pattern of eggs of two groups of species, those regardedas suitable and as unsuitable hosts. The results show that statisticallysignificant differences in the predicted direction existed atthe species level for the interclutch variation between thetwo groups, but not for the intraclutch variation. For 34 speciesfor which the rejection rates of artificial cuckoo eggs wereknown, the degree of variation was compared with the rejectionrates. We found a statistically significant positive relationshipbetween the rejection rate and the degree of interclutch variationin egg appearance, but not between the rejection rate and intraclutchvariation. These results support the idea that there has beena coevolutionary arms race between the cuckoo and its hostsin Europe, leading to a high degree of interclutch variationin egg appearance in passerines. The lack of a trend regardingintraclutch variation is discussed.     

Experimental Manipulation of Intraclutch Variation in the Great Reed Warbler Shows No Effect on Rejection of Parasitic Eggs

In the continuing arms race between hosts and brood parasites, hosts are expected to reduce variation in the appearance of their own eggs within clutches, as it facilitates recognition of parasitic eggs. At the same time, by increasing interclutch variation, hosts should make it more difficult for parasites to evolve perfectly mimetic eggs. In this study, we experimentally manipulated intraclutch variation in the great reed warbler, Acrocephalus arundinaceus, in Hungary, where this species is heavily (c. 64%) parasitized by the common cuckoo, Cuculus canorus. We placed artificial cuckoo eggs, which appeared moderately mimetic to humans, in two groups of nests; in one group we increased variability of egg appearance within clutches by exchanging host eggs among nests. These clutches showed a significantly higher intraclutch variability than natural clutches, which we used as a control group. Our results indicate that it has no effect on rejection behaviour in this species, neither when variation was increased experimentally, nor within the natural range of variation displayed by our population. We suggest that when parasitism is high, selection for reduced intraclutch variation may be less important than frequency‐dependent selection for increased variation between individuals within a host population.     

Experimental Shifts in Intraclutch Egg Color Variation Do Not Affect Egg Rejection in a Host of a Non-Egg-Mimetic Avian Brood Parasite

Avian brood parasites lay their eggs in the nests of other birds, and impose the costs associated with rearing parasitic young onto these hosts. Many hosts of brood parasites defend against parasitism by removing foreign eggs from the nest. In systems where parasitic eggs mimic host eggs in coloration and patterning, extensive intraclutch variation in egg appearances may impair the host’s ability to recognize and reject parasitic eggs, but experimental investigation of this effect has produced conflicting results. The cognitive mechanism by which hosts recognize parasitic eggs may vary across brood parasite hosts, and this may explain variation in experimental outcome across studies investigating egg rejection in hosts of egg-mimicking brood parasites. In contrast, for hosts of non-egg-mimetic parasites, intraclutch egg color variation is not predicted to co-vary with foreign egg rejection, irrespective of cognitive mechanism. Here we tested for effects of intraclutch egg color variation in a host of nonmimetic brood parasite by manipulating egg color in American robins (Turdus migratorius), hosts of brown-headed cowbirds (Molothrus ater). We recorded robins’ behavioral responses to simulated cowbird parasitism in nests where color variation was artificially enhanced or reduced. We also quantified egg color variation within and between unmanipulated robin clutches as perceived by robins themselves using spectrophotometric measures and avian visual modeling. In unmanipulated nests, egg color varied more between than within robin clutches. As predicted, however, manipulation of color variation did not affect rejection rates. Overall, our results best support the scenario wherein egg rejection is the outcome of selective pressure by a nonmimetic brood parasite, because robins are efficient rejecters of foreign eggs, irrespective of the color variation within their own clutch.     

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.     

How precise is egg discrimination in weaverbirds?

The village weaverbird, Ploceus cucullatus, lays eggs of an extremely broad range of appearance between individuals. This variation is thought to have evolved as a counteradaptation to brood parasitism by the diederik cuckooChrysococcyx caprius . The primary objective of our study was to characterize the relationship between egg appearance and egg rejection in the African village weaverbird. We test predictions of three hypotheses in a study in The Gambia, West Africa: (1) interindividual egg variability permits individuals to discriminate between own and foreign eggs by rejecting eggs in proportion to the difference in appearance from their own; (2) village weavers remember the appearance of their own eggs and do not require a discordancy within their clutch, nor even the presence of one of their own eggs, in order to distinguish a foreign egg as such; and (3) colour and speckling contain the signature information by which village weavers can distinguish their eggs from foreign ones; whereas shape and mass, being less reliable, do not. We analysed rejection behaviour according to egg appearance differences by logistic regression. Results supported all three hypotheses. We estimated the predictive efficacy of our model, the amount of explained variation and the relative contribution of various egg appearance factors to discrimination by the host. These results are consistent with the hypothesis that interindividual egg variation in this species facilitates offspring recognition and is a counteradaptation to either interspecific or intraspecific brood parasitism. Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved.     

Variation in offspring size within a population of the web-building spiderAgelena limbata

Within a population of the web-building spiderAgelena limbata, the weight of the first instar nymphs ranged from 1.187 to 6.559 mg. Both intraclutch and interclutch variation were recorded. The mean weights were different among clutches and the coefficients of variation within a clutch ranged from 3.3 to 29.2%. Variation in the nymphal weight was certainly derived from variation in the egg weight because there was a high correlation between the two weights. Factors affecting interclutch variation in nymphal weight were examined by multiple regression analysis. Nymphal weight was positively correlated with the body size and food conditions of female parents, and negatively correlated with the clutch size. Among these three factors, the food conditions of female parents had the largest apparent effect on the interclutch variation. The results suggest that females with larger body size and more food produce larger offspring, and that there is a trade-off between offspring size and clutch size. Heavier nymphs had larger body size (carapace width) and may have larger energy reserves. Heavier nymphs survived experimental starvation for a significantly longer period.     

MAGPIE HOST MANIPULATION BY GREAT SPOTTED CUCKOOS: EVIDENCE FOR AN AVIAN MAFIA?

Why should the hosts of brood parasites accept and raise parasitic offspring that differ dramatically in appearance from their own? There are two solutions to this evolutionary enigma. (1) Hosts may not yet have evolved the capability to discriminate against the parasite, or (2) parasite-host systems have reached an evolutionary equilibrium. Avian brood parasites may either gain renesting opportunities or force their hosts to raise parasitic offspring by destroying or preying upon host eggs or nestlings following host ejection of parasite offspring. These hypotheses may explain why hosts do not remove parasite offspring because only then will hosts avoid clutch destruction by the cuckoo. Here we show experimentally that if the egg of the parasitic great spotted cuckoo Clamator glandarius is removed from nests of its magpie Pica pica host, nests suffer significantly higher predation rates than control nests in which parasite eggs have not been removed. Using plasticine model eggs resembling those of magpies and observations of parasites, we also confirm that great spotted cuckoos that have laid an ejected egg are indeed responsible for destruction of magpie nests with experimentally ejected parasite eggs. Cuckoos benefit from destroying host offspring because they thereby induce some magpies to renest and subsequently accept a cuckoo egg.     

Errors in egg-laying by female Common Cuckoo Cuculus canorus in nests of its common host

Dozens of studies have documented that brood parasites are well adapted to a brood parasitic lifestyle but not all parasitism events are successful. Co-evolution between brood parasites and their hosts is a dynamic process so it is reasonable to expect that a female brood parasite may commit errors during egg deposition by laying her eggs outside the laying period of the host, with consequent impacts on her fitness. Using an extensive dataset from a long-term study, we evaluated egg-laying patterns and errors related to the timing of egg-laying in the Common Cuckoo Cuculus canorus (hereafter ‘Cuckoo’). Specifically, we tested whether the Cuckoo avoids laying before or on the day of host clutch initiation to reduce the risk of rejection of parasitic eggs, whether laying errors will be more frequent in periods with a lack of active host nests, and whether the laying errors will be more frequent in periods with intense Cuckoo parasitism and a consequent lack of suitable host nests. We found that about one-third of Cuckoo eggs were laid on the host clutch initiation day or 1 day before, and the percentage of Cuckoo eggs laid decreased thereafter. Surprisingly, the probability of Cuckoo egg acceptance by the hosts was not affected by the egg-laying stage of the host clutch. Errors in the timing of egg-laying with fatal consequences (i.e. those precluding Cuckoo hatching because of laying in incubated or deserted clutches) were recorded in about 5% of cases. Only laying date of a Cuckoo egg had a significant effect on the probability of errors, which increased during the breeding season. This may be related to the higher number of deserted and incubated host nests at the site at the end of the breeding season. Errors in egg-laying may be attributed to young and inexperienced females but also impaired body condition or intraspecific competition may cause this behaviour. Future studies, which will test these possible explanations, will help to understand better the mechanism of co-evolutionary arms races and differences between host specialist and generalist brood parasites in various host–parasite systems.     

Within‐ and between‐season repeatability of eggshell colouration in the great reed warbler Acrocephalus arundinaceus

While avian eggshell colouration has attracted biologists for decades, little is known about its variation within individuals. The main goal of this study was to explore within‐ and between‐season repeatability of eggshell appearance in the great reed warbler Acrocephalus arundinaceus. To achieve this, we measured eggshell reflectance of first and replacement clutches of individual females within one breeding season, and the reflectance of their first clutches in two following breeding seasons. As environmental conditions may affect egg colouration, repeatability was estimated from linear mixed‐effects models where we initially included temperature and rainfall during egg laying, as well as year, clutch order and egg‐laying date as fixed effects, and clutch identity nested in females as random effects. Eggshell appearance within clutches showed moderate repeatability, while both within‐ and between‐season repeatability in clutch colouration for individual females was low. Our findings indicate that low intra‐clutch variation may have a function within the context of brood parasitism, i.e. in facilitating host recognition of alien eggs. With variable eggs between successive clutches, however, host females may need to relearn the appearance of their eggs with every clutch they lay. This could represent a significant constraint for host egg‐discrimination abilities. Yet, whether environmental or intrinsic physiological factors are responsible for the variation in eggshell colouration between successive clutches of the same females still remain to be discovered.     

How to Spot a Stranger's Egg? A Mimicry‐Specific Discordancy Effect in the Recognition of Parasitic Eggs

Egg discrimination by hosts is an antiparasitic defence to reject foreign eggs from the nest. Even when mimetic, the presence of brood parasitic egg(s) typically alters the overall similarity of all eggs in a clutch, producing a discordant clutch compared to more homogenous clutches of composed only of hosts’ own eggs. In multiple parasitism, the more foreign eggs are laid in the nest, the more heterogeneous the overall clutch appears. Perceptual filters and recognition templates cannot explain the known pattern of lower rejection rates of foreign eggs in multiple vs. single parasitism. We therefore assessed the role of clutch homogeneity and manipulated the colour of one or more eggs in the clutches of great reed warbler (Acrocephalus arundinaceus) hosts of common cuckoos (Cuculus canorus). Varying the colours of both the majority and the minority eggs caused predictable shifts in the rejection of the focal egg(s), and ejection rates of the minority egg colour consistently increased but only when it belonged to a more mimetic egg colour, relative to the less mimetic colour of majority eggs. The results imply that in addition to sensory filters, and template‐based cognitive decision rules, discordancy‐based rejection is affected by the overall clutch appearance and interacts with specific colours varying in the extent of mimicry, to contribute to the recognition decisions of hosts to reject parasitic eggs.     

Evolution of defences against cuckoo (<Emphasis Type="Italic">Cuculus canorus</Emphasis>) parasitism in bramblings (<Emphasis Type="Italic">Fringilla montifringilla</Emphasis>): a comparison of four populations in Fennoscandia

The brood parasitic common cuckoo Cuculus canorus has a history of coevolution that involves numerous passerine hosts, but today only a subset is known to be regularly parasitised in any area. In some hosts, there is significant variation in the occurrence of parasitism between populations, but still individuals in non-parasitised populations show strong antiparasite defences. In the present study we compared the strength of egg rejection of four distant Fennoscandian brambling Fringilla montifringilla populations experiencing different levels of cuckoo parasitism (0–6%). Egg rejection ability was in general very well developed and we did not find any population differences in the relationship between egg rejection probability and similarity between host and experimental parasitic eggs. Furthermore, bramblings very rarely made errors in rejection, indicating that selection against rejection behaviour is likely to be very weak. The brambling-cuckoo system therefore differs from other well studied systems which are characterised by pronounced spatial and temporal variation in the host’s level of defence. This result is unlikely to reflect independent replication of the same evolutionary trajectory because the weak breeding site tenacity of bramblings should result in an extreme amount of gene flow within the distribution area and thus strongly impede localised responses to selection. Instead, lack of geographic variation has more likely arisen because bramblings respond to selection as one evolutionary unit, and because the average parasitism pressures have been high enough in the past to cause regional fixation of rejection alleles and evolution of clutch characteristics that facilitate cost free egg recognition.     

The evolution of different maternal investment strategies in two closely related desert vertebrates

We compared egg size phenotypes and tested several predictions from the optimal egg size (OES) and bet‐hedging theories in two North American desert‐dwelling sister tortoise taxa, Gopherus agassizii and G. morafkai, that inhabit different climate spaces: relatively unpredictable and more predictable climate spaces, respectively. Observed patterns in both species differed from the predictions of OES in several ways. Mean egg size increased with maternal body size in both species. Mean egg size was inversely related to clutch order in G. agassizii, a strategy more consistent with the within‐generation hypothesis arising out of bet‐hedging theory or a constraint in egg investment due to resource availability, and contrary to theories of density dependence, which posit that increasing hatchling competition from later season clutches should drive selection for larger eggs. We provide empirical evidence that one species, G. agassizii, employs a bet‐hedging strategy that is a combination of two different bet‐hedging hypotheses. Additionally, we found some evidence for G. morafkai employing a conservative bet‐hedging strategy. (e.g., lack of intra‐ and interclutch variation in egg size relative to body size). Our novel adaptive hypothesis suggests the possibility that natural selection favors smaller offspring in late‐season clutches because they experience a more benign environment or less energetically challenging environmental conditions (i.e., winter) than early clutch progeny, that emerge under harsher and more energetically challenging environmental conditions (i.e., summer). We also discuss alternative hypotheses of sexually antagonistic selection, which arise from the trade‐offs of son versus daughter production that might have different optima depending on clutch order and variation in temperature‐dependent sex determination (TSD) among clutches. Resolution of these hypotheses will require long‐term data on fitness of sons versus daughters as a function of incubation environment, data as yet unavailable for any species with TSD.