High frequency of multiple paternity in the largest rookery of Mediterranean loggerhead sea turtles

Mating systems are a central component in the evolution of animal life histories and in conservation genetics. The patterns of male reproductive skew and of paternal shares in batches of offspring, for example, affect genetic effective population size. A prominent characteristic of mating systems of sea turtles seem to be a considerable intra- and interspecific variability in the degree of polyandry. Because of the difficulty of observing the mating behaviour of sea turtles directly in the open sea, genetic paternity analysis is particularly useful for gaining insights into this aspect of their reproductive behaviour. We investigated patterns of multiple paternity in clutches of loggerhead sea turtles in the largest Mediterranean rookery using four highly variable microsatellite loci. Furthermore, we tested for a relationship between the number of fathers detected in clutches and body size of females. More than one father was detected in the clutches of 14 out of 15 females, with two clutches revealing the contribution of at least five males. In more than half the cases, the contributions of different fathers to a clutch did not depart from equality. The number of detected fathers significantly increased with increasing female body size. This relationship indicates that males may prefer to mate with large, and therefore productive, females. Our results suggest that polyandry is likely to increase effective population size compared to a population in which females would mate with only one male; male reproductive contributions being equal.     

Females Paired with New and Heavy Mates Reduce Intra-Clutch Differences in Resource Allocation

Reproductive investment affects both offspring and parental fitness and influences the evolution of life histories. Females may vary their overall primary reproductive effort in relation to the phenotypic characteristics of their mate. However, the effects of male quality on differential resource allocation within clutches have been largely neglected despite the potential implications for mate choice and population dynamics, especially in species exhibiting biparental care and brood reduction. Female southern rockhopper penguins Eudyptes chrysocome paired with heavy mates reduced intra-clutch variation in egg and albumen masses. Females paired with new mates also reduced intra-clutch variation in yolk androgen levels. Since both an increased mass and increased androgen concentrations positively influence chick survival under sibling competition, the chances of fledging the whole clutch are likely to be higher for newly formed pairs with heavy males than for previously formed pairs with light males. Interestingly, total clutch provisioning did not vary with male quality. We show for the first time that females vary intra-clutch variation in resource allocation according to male quality. In species with brood reduction, it may be more adaptive for females to modulate the distribution of resources within the clutch according to breeding conditions, than to change their total clutch provisioning.     

Sexual selection when fertilization is not guaranteed

Abstract Much of the theory of sexual selection assumes that females do not generally experience difficulties getting their eggs fertilized, yet sperm limitation is occasionally documented. How often does male limitation form a selection for female traits that improve their mating rate? The question is difficult to test, because if such traits evolve to be efficient, sperm limitation will no longer appear to be a problem to females. Here, we suggest that changes in choosiness between populations, and in particular between virgin and mated females, offer an efficient way to test this hypothesis. We model the “wallflower effect,” that is, changes in female preferences due to time and mortality costs of remaining unmated (for at least some time). We show that these costs cause adaptive reductions of female choice, even if mate encounter rates appear high and females only rarely end their lives unfertilized. We also consider the population consequences of plastic or fixed mate preferences at different mate encounter rates. If mate choice is plastic, we confirm earlier verbal models that virgins should mate relatively indiscriminately, but plastic increase of choosiness in later matings can compensate and intensify sexual selection on the male trait, particularly if there is last male sperm precedence. Plastic populations will cope well with unusual conditions: eagerness of virgins leads to high reproductive output and a relaxation of sexual selection at low population densities. If females lack such plasticity, however, population‐wide reproductive output may be severely reduced, whereas sexual selection on male traits remains strong.     

Sex allocation and clutch size in parasitoid wasps that produce single-sex broods

The parasitoid wasp genus Achrysocharoides (Eulophidae) is unusual in that many of its species lay male and female eggs in single-sex clutches. The average clutch size of female broods is always greater than that of male broods, and in some species male clutch size is always one. We constructed models that predicted that severely egg-limited wasps should produce equal numbers of male and female eggs while severely host-limited wasps should produce equal numbers of male and female broods (and hence an overall female-biased sex ratio). Theory is developed to predict clutch size and sex ratio across the complete spectrum of host and egg limitation. A comparison of 19 surveys of clutch composition in seven species of Achrysocharoides showed a general pattern of equal numbers of male and female broods with a female-biased sex ratio (suggesting host limitation) although with considerable heterogeneity amongst collections and with a number of cases of unexpectedly low frequencies of male broods. Using a previous estimate of the relationship between fitness and size in the field, we predicted the maximally productive (Lack) clutch size for female broods of Achrysocharoides zwoelferi to be three. Of clutches observed in nature, 95% were equal to or smaller in size than the predicted Lack clutch size. When we manipulated local host density in the field, and as predicted by our models, clutch size and the proportion of female broods of A. zwoelferi decreased as hosts became more common, but the absolute frequency of male clutches was lower than expected. Copyright 1998 The Association for the Study of Animal Behaviour.     

Does divergence in female mate choice affect male size distributions in two cave fish populations?

Sexual selection by female choice can maintain male traits that are counter selected by natural selection. Alteration of the potential for sexual selection can thus lead to shifts in the expression of male traits. We investigated female mate choice for large male body size in a fish (Poecilia mexicana) that, besides surface streams, also inhabits two caves. All four populations investigated, exhibited an ancestral visual preference for large males. However, only one of the cave populations also expressed this female preference in darkness. Hence, the lack of expression of female preference in darkness in the other cave population leads to relaxation of sexual selection for large male body size. While P. mexicana populations with size-specific female mate choice are characterized by a pronounced male size variation, the absence of female choice in one cave coincides with the absence of large bodied males in that population. Our results suggest that population differences in the potential for sexual selection may affect male trait variation.     

How host size may constrain the evolution of parasite body size and clutch size. The parasitic isopod Ichthyoxenus fushanensis and its host fish, Varicorhinus bacbatulus, as an example

The flesh-burrowing parasitic isopod Ichthyoxenus fushanensis was found infecting the body cavity of a freshwater fish, Varicorhinus bacbatulus , in heterosexual pairs. Herein we investigate the question of how the host body size may constrain the parasite size and clutch size by analyzing the interactions among the body size and clutch size of the parasite, and host size. Due to the low transmission rate of I. fushanensis to its host and the positive relationship between clutch size and female size, selection may favor larger females with larger clutch sizes to compensate for massive losses of manca (the free-living juveniles). The path model reveals that clutch size depends not only directly on female size, but also on the sizes of her host and mate. Female size also depends on the sizes of the host and her mate. A negative correlation exists between the body sizes of the paired males and females. This negative correlation may be regarded as a consequence of competition for limited available space or other resources provided by the host. The effects of host size on parasite size, however, act on the total volume of both sexes as a whole, not specifically on either the female or the male. In this case, the available space/resources may not allow both individuals of different sexes to evolve toward a larger size simultaneously. Under the constraint of host size, a strategy of reducing the body size of the paired male may provide a way to increase the body size of the paired female and achieve a larger clutch size.     

Male size determines reproductive output in a paternal mouthbrooding fish

Size can have strong effects on reproductive success in both males and females, and in many species large individuals are preferred as mates. To estimate the potential benefits from mate choice for size in both sexes, I studied the effects of the size of each sex on the reproductive output of pairs of Banggai cardinalfish, Pterapogon kauderni, a sexually monomorphic obligate paternal mouthbrooder. When pairs were allowed to form freely, a size-assortative mating pattern was observed and larger pairs had a higher reproductive output as determined by total clutch weight and egg size. To separate the potential benefits from mate choice for size for each sex, I subsequently used these pairs to form reversed size-assortative pairs, that is, the largest male paired to the smallest female and vice versa. I found a positive correlation between male size and clutch size: relatively heavier clutches were found in pairs where females were given a larger male. This suggests that the size of the male influences clutch weight. For egg size, however, the size of both sexes seemed important. The study reveals the benefits of mutual mate choice on size in this species: larger females provide larger eggs and larger males can brood heavier clutches. Furthermore, these results suggest that females differentially allocate resources into the eggs according to the size of the mate.Copyright 2002 The Association for the Study of Animal Behaviour. Published by Elsevier Science Ltd. All rights reserved .     

Mating preference of female zebrafish, Danio rerio, in relation to male dominance

Mating success tends to be skewed toward dominant males, thoughfemale mate preferences may not always correlate with male dominance.In this study, we investigated the mating preferences of femalezebrafish, Danio rerio, in the absence of male–male competition.We paired females sequentially with males of known dominancerank, using a nested, repeated measures design, with egg productionas a measure of female mate preference. We predicted that femaleswould spawn more frequently and produce larger clutches whenpaired with males of higher dominance rank. We found significantdifferences among females in the size of clutches produced andamong males in the size of clutches received, but these differenceswere independent of male dominance rank. Male body size wasnot related to either dominance rank or clutch size received.These results indicate that females vary clutch size in relationto the males with which they are paired but that they do notfavor dominant males. Thus, male competition may normally overridefemale mate preference in zebrafish.     

Paternal care and male mate-attraction effort in the European starling is adjusted to clutch size

In facultative polygynous birds with biparental care, a trade-off may occur between male parental care and attraction of additional mates. If there is a cost associated with reduced male parental care, the relative benefit of mate attraction may be predicted to decrease as the size of a male's clutch or brood increases. We tested this prediction in monogamous pairs of facultatively polygynous European starlings (Sturnus vulgaris). The larger the clutch, the more time the male spent incubating and the less time he spent attracting an additional female (i.e. singing near and carrying green nesting material into adjacent empty nest-boxes). Reduced paternal incubation resulted in lower overall incubation (the female did not compensate) and lower hatching success. Immediately after experimental reduction of clutches, males spent significantly less time incubating and more time singing and carrying greenery, and vice versa for experimentally enlarged clutches. Males with experimentally reduced clutches attracted a second female more often than males with experimentally enlarged clutches. This is the first study, to our knowledge, to provide experimental evidence for an adjustment of paternal care and male mate-attraction effort to clutch size. However, a trade-off between paternal nestling provisioning and mate attraction was not revealed, probably due to the absence of unpaired females by that time in the breeding season. Experiments showed that the relative contribution of the male and female to nestling provisioning was unrelated to brood size.     

Clutch size evolution under sexual conflict enhances the stability of mating systems.

Models of optimal clutch size often implicitly assume a situation with uniparental care. However, the evolutionary conflict between males and females over the division of parental care will have a major influence on the evolution of clutch size. Since clutch size is a female trait, a male has little possibility of directly influencing it. However, the optimal clutch size from a female's perspective will depend on the amount of paternal care her mate is expected to provide. The sexual conflict over parental care will in its turn be affected by clutch size, since a larger clutch makes male care more valuable. Hence, there will be joint evolution of mating system and clutch size. In this paper, we demonstrate that this joint evolution will tend to stabilize the mating system. In a situation with conventional sex roles, this joint evolution might result in either increased clutch size and biparental care or reduced clutch size and uniparental female care. Under some circumstances the initial conditions might determine which will be the outcome. These results demonstrate that it may be difficult to deduce whether biparental care evolved because of few opportunities for breeding males increasing their fitness by attracting additional mates or because of the importance of male care for offspring fitness by studying prevailing mating systems using, for example, male removals or manipulation of males' opportunities for finding additional mates. In general terms, we demonstrate that models of life-history evolution have to consider the social context in which they evolve.     

Life-history variation of a neotropical thrush challenges food limitation theory

Since David Lack first proposed that birds rear as many young as they can nourish, food limitation has been accepted as the primary explanation for variation in clutch size and other life-history traits in birds. The importance of food limitation in life-history variation, however, was recently questioned on theoretical grounds. Here, we show that clutch size differences between two populations of a neotropical thrush were contrary to expectations under Lack's food limitation hypothesis. Larger clutch sizes were found in a population with higher nestling starvation rate (i.e. greater food limitation). We experimentally equalized clutches between populations to verify this difference in food limitation. Our experiment confirmed greater food limitation in the population with larger mean clutch size. In addition, incubation bout length and nestling growth rate were also contrary to predictions of food limitation theory. Our results demonstrate the inability of food limitation to explain differences in several life-history traits: clutch size, incubation behaviour, parental feeding rate and nestling growth rate. These life-history traits were better explained by inter-population differences in nest predation rates. Food limitation may be less important to life history evolution in birds than suggested by traditional theory.     

Can sexual selection drive female life histories? A comparative study on Galliform birds

Sexual selection has been identified as a major evolutionary force shaping male life history traits but its impact on female life history evolution is less clear. Here we examine the impact of sexual selection on three key female traits (body size, egg size and clutch size) in Galliform birds. Using comparative independent contrast analyses and directional discrete analyses, based on published data and a new genera-level supertree phylogeny of Galliform birds, we investigated how sexual selection [quantified as sexual size dimorphism (SSD) and social mating system (MS)] affects these three important female traits. We found that female body mass was strongly and positively correlated with egg size but not with clutch size, and that clutch size decreased as egg size increased. We established that SSD was related to MS, and then used SSD as a proxy of the strength of sexual selection. We found both a positive relationship between SSD and female body mass and egg size and that increases in female body mass and egg size tend to occur following increases in SSD in this bird order. This pattern of female body mass increases lagging behind changes in SSD, established using our directional discrete analysis, suggests that female body mass increases as a response to increases in the level of sexual selection and not simply through a strong genetic relationship with male body mass. This suggests that sexual selection is linked to changes in female life history traits in Galliformes and we discuss how this link may shape patterns of life history variation among species.     

ASPECTS OF THE BREEDING BIOLOGY OF THE FIERYNECKED NIGHTJAR

Jackson H. D. 1985. Aspects of the breeding biology of the Fierynecked Nightjar. Ostrich 56: 263–276.

A marked population of nightjars in Zimbabwe was studied intensively for four breeding seasons. This paper covers certain aspects of the breeding biology of the Fierynecked Nightjar Caprimulgus pectoralis. The male shows strong site fidelity during the breeding season (September to December), singing, feeding and breeding within an area of about 5,8 ha. There is some evidence of site defence by the male. The female shows strong mate fidelity, resulting in a pair bond for life. Egg laying starts with full moon in September and is further stimulated by the next two full moon periods. The eggs are laid directly on dense leaf litter at a site overhung by foliage. The normal clutch is two eggs (12S % are one egg) laid on successive days during the afternoon. Incubation starts with the first egg and is by the male at night and the female by day. The incubation period is 18 days. The birds respond to undue disturbance by deserting the eggs and laying a replacement clutch. The chicks usually hatch on successive afternoons; they are mobile on the first day and will move to a parent if called. Both parents feed and brood the young during twilight and moonlight; the male broods them on dark nights and the female does so by day. The species is double-brooded when time permits, the female laying again once the first brood has reached independence; she may even lay a third clutch if the second one comes to grief. There is no evidence of adults transporting eggs or young.     

The context-dependent effect of multiple paternity on effective population size

Effective population size (N(e)) is important because it describes how evolutionary forces will affect a population. The effect of multiple sires per female on N(e) has been the subject of some debate, at the crux of which is the effects of monandry and multiple-paternity (MP) on male variance in reproductive success. In both mating systems, females mate with several males over their lifetimes, but sire offspring with one male at a time in the former and have several sires per clutch in the latter. First, I theoretically show that whether the annual male variance in reproductive success in an MP population is greater or less than that of a monandrous population depends on the distributions of within-clutch paternity. Then, I simulated different distributions of within-clutch paternity under a range of parameters that characterize natural populations to show that an MP population can have an N(e) smaller or larger than that of a monandrous population with otherwise equal dynamics. The N(e(MP)):N(e(Monandry)) ratio increased with mating frequency and female variance in reproductive success, was equalized by long generation times, and was affected by the distribution of within-clutch paternities. The results of this model provide a unifying framework for the debate.     

Life history patterns in lizards of the arid and semiarid zone of Australia

Summary Studies on the life histories and population dynamics of lizards in the semiarid/arid zone of Australia are reviewed to identify the influence of size (female mean snout-vent length), phylogeny (family effects) and ecological parameters on the evolution of life history traits of these species. Species producing more than one clutch per year are larger than single-clutched ones. In an ANCOVA, significant effects of size and phylogeny on clutch size and on age at sexual maturity were found. Microhabitat (arboreal, terrestrial, and subterranean life style) also had an effect on clutch size, but only mediated through a significant interaction with size. However, results of the ANCOVAs depend on the families and ecological parameters included in the analyses. Therefore, caution is necessary in interpreting or generalizing the results; in any case, size and phylogeny explain only a small percentage of the observed variation. Nevertheless, a direct comparison of a set of syntopic/paratopic desert lizards supports and extends the main conclusions of the ANCOVA. A significant but small phylogenetic effect was found, and arboreal microhabitat was associated with greater age at sexual maturity. Activity (diurnal versus nocturnal) influenced yearly mortalities and clutch frequencies. For both, microhabitat and activity, predation levels and size-dependent mortality were the likely selective factors causing these correlations. The demographic environment explains the paucity of duurnal lizard species with fixed clutch sizes in the semiarid/arid zone of Australia. Possible causes for the evolution of fixed clutch sizes are discussed.     

Reproductive senescence and dynamic oviposition behaviour in insects

We explore the relationship between clutch size behaviour and the likelihood of egg limitation in insects with parasitoid-like life histories. We compare the incidence of egg limitation in insects that produce clutch sizes consistent with maximizing fitness per host (i.e. the single host maximum, or Lack clutch size) with insects exhibiting two types of dynamic behaviour. In the first case, insects produce clutch sizes according to a rule that specifies a negative relationship between egg complement and clutch size; in the second case, clutch size is determined by both egg complement and the host encounter rate using a dynamic state-variable model. The analyses are an extension of models presented by Rosenheim (1996), which predicted a strong positive relationship between the risk of egg limitation and the host encounter rate in the absence of dynamic oviposition behaviour. Our results are consistent with Rosenheim's, but they show that dynamic behaviour can greatly reduce th e risk of egg limitation and weaken the relationship between the host encounter rate and egg limitation.     

Life history alterations upon oral and hemocoelic bacterial exposure in the butterfly Melitaea cinxia

Life history strategies often shape biological interactions by specifying the parameters for possible encounters, such as the timing, frequency, or way of exposure to parasites. Consequentially, alterations in life‐history strategies are closely intertwined with such interaction processes. Understanding the connection between life‐history alterations and host–parasite interactions can therefore be important to unveil potential links between adaptation to environmental change and changes in interaction processes. Here, we studied how two different host–parasite interaction processes, oral and hemocoelic exposure to bacteria, affect various life histories of the Glanville fritillary butterfly Melitaea cinxia. We either fed or injected adult butterflies with the bacterium Micrococcus luteus and observed for differences in immune defenses, reproductive life histories, and longevity, compared to control exposures. Our results indicate differences in how female butterflies adapt to the two exposure types. Orally infected females showed a reduction in clutch size and an earlier onset of reproduction, whereas a reduction in egg weight was observed for hemocoelically exposed females. Both exposure types also led to shorter intervals between clutches and a reduced life span. These results indicate a relationship between host–parasite interactions and changes in life‐history strategies. This relationship could cast restrictions on the ability to adapt to new environments and consequentially influence the population dynamics of a species in changing environmental conditions.     

Single and multiple mating reduces longevity of female dumpling squid (Euprymna tasmanica)

For many species, mating is a necessary yet costly activity. The costs involved can have an important influence on the evolution of life histories and senescence. Females of many species mate multiply, and this behaviour can inflict a longevity cost. Most studies investigating the effects of multiple mating on female survival have been conducted on insects, and the effects in other taxa are largely unknown. We investigate the effects of both a single mating and a second mating on longevity in female dumpling squid (Euprymna tasmanica), a species in which both sexes mate multiply. Through comparing the longevity of virgin, once‐mated and twice‐mated females, we found that a single mating reduced female life span by 15 days on average. A second mating resulted in an additional 8 day (on average) longevity cost, despite no difference in total clutch mass, number of clutches, single egg mass or number of eggs per clutch between once‐mated and twice‐mated females. This demonstrates a cost to multiple mating which may be independent of the cost of egg production. Furthermore, total clutch mass and female life span were positively correlated, whereas female life span decreased with increasing average water temperature. The presence of an additive effect of reproduction on longevity suggests that multiple mating in cephalopods may have benefits that outweigh these costs, or that there is a conflict in optimal mating frequency between males and females.     

Male attractiveness regulates daughter fecundity non-genetically via maternal investment

Mothers can non-genetically influence offspring phenotype in response to environmental conditions, including mate attractiveness. If such 'maternal effects' influence the offspring's reproduction and F2 generation, there is a mechanism for non-genetic trans-generational effects on phenotype, including epigenetic phenomena, with implications for evolution and population dynamics. We demonstrate in the zebra finch Taeniopygia guttata such non-genetic effects on offspring fecundity and the size of early stage F2 (eggs) in response to experimentally manipulated father's attractiveness. Our experimental design allowed us to deduce that the mechanism for this non-genetic paternal effect was via maternal investment in eggs. This affected female offspring size and, consequently, fecundity and F2 (egg) size. This demonstrates that female perception of mate attractiveness can have non-genetic, trans-generational fitness consequences and this may have important implications for the evolution of sexually selected traits and population dynamics.     

Population ecology and life history of the diurnal skink Morethia boulengeri in arid Australia

Summary The life history and population ecology of the skink Morethia boulengeri were studied from September 1985 to May 1987 in populations in a riverine woodland habitat and at an abandoned homestead in Kinchega National Park. The population dynamics and life histories of the two populations were remarkably similar. Yearly mortality (including emigration) ranged from 0.84–0.89. The yearly emigration rate was 0.01–0.03. Size-and body-condition-dependent mortality could be demonstrated for the population in riverine woodland. Average spring time densities were similar in both study sites but varied between years and ranged from 421-1823 individuals/ha. M. boulengeri females laid on average 2.8 eggs per clutch and usually produced three clutches per year. Egg mass was significantly correlated with female snout-vent-length, but relative clutch mass and egg size were not. All surviving juveniles reproduced for the first time in their first year. Some activity occurred throughout the year. Preferred body temperatures decreased in the cooler months. The data fit demographic models of life history evolution.