Human fertility in relation to education, economy, religion, contraception, and family planning programs.

BACKGROUND: The world population is expected to increase greatly this century, aggravating current problems related to climate, health, food security, biodiversity, energy and other vital resources. Population growth depends strongly on total fertility rate (TFR), but the relative importance of factors that influence fertility needs more study. METHODS: We analyze recent levels of fertility in relation to five factors: education (mean school years for females), economy (Gross Domestic Product, GDP, per capita), religiosity, contraceptive prevalence rate (CPR), and strength of family planning programs. We compare six global regions: E Europe, W Europe and related countries, Latin America and the Caribbean, the Arab States, Sub-Saharan Africa, and Asia. In total, 141 countries are included in the analysis. We estimate the strength of relationships between TFR and the five factors by correlation or regression and present the results graphically. RESULTS: In decreasing order of strength, fertility (TFR) correlates negatively with education, CPR, and GDP per capita, and positively with religiosity. Europe deviates from other regions in several ways, e.g. TFR increases with education and decreases with religiosity in W Europe. TFR decreases with increasing strength of family planning programs in three regions, but only weakly so in a fourth, Sub-Saharan Africa (the two European regions lacked such programs). Most factors correlated with TFR are also correlated with each other. In particular, education correlates positively with GDP per capita but negatively with religiosity, which is also negatively related to contraception and GDP per capita. CONCLUSIONS: These results help identify factors of likely importance for TFR in global regions and countries. More work is needed to establish causality and relative importance of the factors. Our novel quantitative analysis of TFR suggests that religiosity may counteract the ongoing decline of fertility in some regions and countries.

Brood parasitism, relatedness and sociality: a kinship role in female reproductive tactics.

Conspecific brood parasitism (CBP) is a reproductive tactic in which parasitic females lay eggs in nests of other females of the same species that then raise the joint brood. Parasites benefit by increased reproduction, without costs of parental care for the parasitic eggs. CBP occurs in many egg-laying animals, among birds most often in species with large clutches and self-feeding young: two major factors facilitating successful parasitism. CBP is particularly common in waterfowl (Anatidae), a group with female-biased natal philopatry and locally related females. Theory suggests that relatedness between host and parasite can lead to inclusive fitness benefits for both, but if host costs are high, parasites should instead target unrelated females. Pairwise relatedness (r) in host-parasite (h-p) pairs of females has been estimated using molecular genetic methods in seven waterfowl (10 studies). In many h-p pairs, the two females were unrelated (with low r, near the local population mean). However, close relatives (r = 0.5) were over-represented in h-p pairs, which in all 10 studies had higher mean relatedness than other females. In one species where this was studied, h-p relatedness was higher than between nesting close neighbours, and hosts parasitized by non-relatives aggressively rejected other females. In another species, birth nest-mates (mother-daughters, sisters) associated in the breeding area as adults, and became h-p pairs more often than expected by chance. These and other results point to recognition of birth nest-mates and perhaps other close relatives. For small to medium host clutch sizes, addition of a few parasitic eggs need not reduce host offspring success. Estimates in two species suggest that hosts can then gain inclusive fitness if parasitized by relatives. Other evidence of female cooperation is incubation by old eider Somateria mollissima females of clutches laid by their relatives, and merging and joint care of broods of young. Merging females tended to be more closely related. Eiders associate with kin in many situations, and in some geese and swans, related females may associate over many years. Recent genetic evidence shows that also New World quails (Odontophoridae) have female-biased natal philopatry, CBP and brood merging, inviting further study and comparison with waterfowl. Kin-related parasitism also occurs in some insects, with revealing parallels and differences compared to birds. In hemipteran bugs, receiving extra eggs is beneficial for hosts by diluting offspring predation. In eggplant lace bugs Gargaphia solani, host and parasite are closely related, and kin selection favours egg donation to related females. Further studies of kinship in CBP, brood merging and other contexts can test if some of these species are socially more advanced than presently known.

Helping Relatives Survive and Reproduce: Inclusive Fitness and Reproductive Value in Brood Parasitism.

Costly help can raise a relative's reproduction, survival, and reproductive value and increase the inclusive fitness of the donor of help. Donor fitness is explored here in conspecific brood parasitism. In this alternative reproductive tactic, some females, "parasites," lay eggs in nests of other females of the same species, "hosts," suppliers of help that alone take care of the offspring. Modeling shows that hosts can gain inclusive fitness if parasitized by relatives whose reproduction or survival is thereby increased. These predictions are explored in waterfowl with frequent brood parasitism, female-biased philopatry, and neighbor relatedness. Approximate estimates based on waterfowl reproductive and life-history data show that host inclusive-fitness gain is often possible with related parasites. The largest gains can be achieved through increased reproduction, but gain is also possible through higher survival of parasites that avoid increased predation and other risks of nesting. Inclusive fitness depends on parasite reproductive value and can be highest for a host parasitized by her mother and for old, senescent hosts with low fecundity, helping young related parasites. These results and observed levels of host-parasite relatedness suggest that being "parasitized" in waterfowl is sometimes neutral or even advantageous because of inclusive-fitness benefits, contributing to evolution of frequent conspecific brood parasitism in this group.

Don't put all your eggs in one nest: spread them and cut time at risk.

In many egg-laying animals, some females spread their clutch among several nests. The fitness effects of this reproductive tactic are obscure. Using mathematical modeling and field observations, we analyze an unexplored benefit of egg spreading in brood parasitic and other breeding systems: reduced time at risk for offspring. If a clutch takes many days to lay until incubation and embryo development starts after the last egg, by spreading her eggs a parasitic female can reduce offspring time in the vulnerable nest at risk of predation or other destruction. The model suggests that she can achieve much of this benefit by spreading her eggs among a few nests, even if her total clutch is large. Field data from goldeneye ducks Bucephala clangula show that egg spreading enables a fecund female to lay a clutch that is much larger than average without increasing offspring time at risk in a nest. This advantage increases with female condition (fecundity) and can markedly raise female reproductive success. These results help explain the puzzle of nesting parasites in some precocial birds, which lay eggs in the nests of other females before laying eggs in their own nest. Risk reduction by egg spreading may also play a role in the evolution of other breeding systems and taxa-for instance, polyandry with male parental care in some birds and fishes.

Inclusive fitness theory and eusociality.

Arising from M. A. Nowak, C. E. Tarnita & E. O. Wilson 466, 1057-1062 (2010); Nowak et al. reply. Nowak et al. argue that inclusive fitness theory has been of little value in explaining the natural world, and that it has led to negligible progress in explaining the evolution of eusociality. However, we believe that their arguments are based upon a misunderstanding of evolutionary theory and a misrepresentation of the empirical literature. We will focus our comments on three general issues.

Indeterminate laying and flexible clutch size in a capital breeder, the common eider.

Clutch size control in capital breeders such as large waterfowl has been much debated. Some studies have concluded that clutch size in ducks is determined before the start of laying and does not change in response to egg additions or removals. The response, however, may depend on the timing of tests, and experiments may have been too late for females to alter the number of eggs. We here study clutch size responses to predation of first and second eggs in the common eider, using protein fingerprinting of egg albumen to verify that the same female continues laying in the nest after predation. Sixty of 79 females with early egg predation (one or both of the two first eggs) deserted the nest. Among the 19 females that stayed and continued laying, the mean number of eggs produced was 4.4, significantly higher than the 3.7 in non-predated nests. The staying females had similar egg size and clutch initiation date as females that deserted, and their body mass and clutch initiation date was similar to that of females whose clutches were not predated. Even capital-breeding common eiders may therefore be indeterminate layers, as many females in which early eggs are removed lay more eggs than others. A previous study has shown that they can reduce their laying if eggs are added. Our results add to increasing evidence that ducks have more flexible egg production than previously thought.

Colony kin structure and host-parasite relatedness in the barnacle goose.

Conspecific brood parasitism (CBP), females laying eggs in the nest of other 'host' females of the same species, is a common alternative reproductive tactic among birds. For hosts there are likely costs of incubating and rearing foreign offspring, but costs may be low in species with precocial chicks such as waterfowl, among which CBP is common. Waterfowl show strong female natal philopatry, and spatial relatedness among females may influence the evolution of CBP. Here we investigate fine-scale kin structure in a Baltic colony of barnacle geese, Branta leucopsis, estimating female spatial relatedness using protein fingerprints of egg albumen, and testing the performance of this estimator in known mother-daughter pairs. Relatedness was significantly higher between neighbour females (nesting < or = 40 metres from each other) than between females nesting farther apart, but there was no further distance trend in relatedness. This pattern may be explained by earlier observations of females nesting close to their mother or brood sisters, even when far from the birth nest. Hosts and parasites were on average not more closely related than neighbour females. In 25 of 35 sampled parasitized nests, parasitic eggs were laid after the host female finished laying, too late to develop and hatch. Timely parasites, laying eggs in the host's laying sequence, had similar relatedness to hosts as that between neighbours. Females laying late parasitic eggs tended to be less related to the host, but not significantly so. Our results suggest that CBP in barnacle geese might represent different tactical life-history responses.

Host-parasite kinship in a female-philopatric bird population: evidence from relatedness trend analysis.

Conspecific brood parasitism (CBP), an alternative reproductive tactic where some females lay eggs in the nests of other females of the same species, occurs in many animals with egg care. It is particularly common in waterfowl, for reasons that are debated. Many waterfowl females nest near their birthplace, making it likely that some local females are relatives. We analyse brood parasitism in a Hudson Bay population of common eiders, testing predictions from two alternative hypotheses on the role of relatedness in CBP. Some models predict host-parasite relatedness, others predict that parasites avoid close relatives as hosts. To distinguish between the alternatives, we use a novel approach, where the relatedness of host-parasite pairs is tested against the spatial population trend in pairwise relatedness. We estimate parasitism, nest take-over and relatedness with protein fingerprinting and bandsharing analysis of egg albumen, nondestructively sampled from each new egg in the nest throughout the laying period. The results refute the hypothesis that parasites avoid laying eggs in the nests of related hosts, and corroborate the alternative of host-parasite relatedness. With an estimated r of 0.12-0.14, females laying eggs in the same nest are on average closer kin than nesting neighbour females. Absence of a population trend in female pairwise relatedness vs. distance implies that host-parasite relatedness is not only an effect of strong natal philopatry: some additional form of kin bias is also involved.

Sexual selection and mate choice.

The past two decades have seen extensive growth of sexual selection research. Theoretical and empirical work has clarified many components of pre- and postcopulatory sexual selection, such as aggressive competition, mate choice, sperm utilization and sexual conflict. Genetic mechanisms of mate choice evolution have been less amenable to empirical testing, but molecular genetic analyses can now be used for incisive experimentation. Here, we highlight some of the currently debated areas in pre- and postcopulatory sexual selection. We identify where new techniques can help estimate the relative roles of the various selection mechanisms that might work together in the evolution of mating preferences and attractive traits, and in sperm-egg interactions.

Reproductive tactics under severe egg predation: an eider's dilemma.

Parental defence against predators may increase offspring survival but entail other costs. Egg predation is frequent early in the laying sequence of the common eider, which differs in this and in several other ways from most other waterfowl. We test the hypothesis that permanent presence at the nest from the second or third egg is an adaptation for reducing egg predation in eiders. Two other alternative hypotheses for lower predation at later nest stages are early predation loss of the most vulnerable nests and seasonal decrease in predation risk. Analyses of predation rates at the one-egg and later stages refute these two alternatives. Early nest attendance by eider females is estimated to increase clutch survival by about 20% in four-egg and 35% in five-egg clutches, albeit probably at a cost of smaller clutch size.

Predation by sparrowhawks decreases with increased breeding density in a songbird, the great tit.

Predators may regulate prey populations if predation rate increases with prey density. Alternatively, if space-limited (e.g. territorial) predators become 'satiated' when prey exceed a certain density, increased prey abundance may lead to reduced predation rate. These alternatives have been difficult to test experimentally for mobile prey in the wild. We present such a test, manipulating the density of great tits (Parus major) by adding nest boxes in territories of sparrowhawks (Accipiter nisus). Predation rate was measured for young tits after they left the nests. Although the great tit is an important prey, there was no evidence for regulation during the breeding season: the rate of hawk predation declined with increasing density of tits. This result was not confounded by changes in breeding density of alternative prey species (other songbirds). Hawk predation can therefore favour dense breeding in a territorial (solitary) bird, and conspecific attraction and aggregation reported in several territorial species may partly result from predation pressure. This result also has potential implications for conservation work.

Social polyandry, parental investment, sexual selection, and evolution of reduced female gamete size.

Sexual selection in the form of sperm competition is a major explanation for small size of male gametes. Can sexual selection in polyandrous species with reversed sex roles also lead to reduced female gamete size? Comparative studies show that egg size in birds tends to decrease as a lineage evolves social polyandry. Here, a quantitative genetic model predicts that female scrambles over mates lead to evolution of reduced female gamete size. Increased female mating success drives the evolution of smaller eggs, which take less time to produce, until balanced by lowered offspring survival. Mean egg size is usually reduced and polyandry increased by increasing sex ratio (male bias) and maximum possible number of mates. Polyandry also increases with the asynchrony (variance) in female breeding start. Opportunity for sexual selection increases with the maximum number of mates but decreases with increasing sex ratio. It is well known that parental investment can affect sexual selection. The model suggests that the influence is mutual: owing to a coevolutionary feedback loop, sexual selection in females also shapes initial parental investment by reducing egg size. Feedback between sexual selection and parental investment may be common.

Genetic similarity between mates and extra-pair parentage in three species of shorebirds.

Matings between close relatives often reduce the fitness of offspring, probably because homozygosity leads to the expression of recessive deleterious alleles. Studies of several animals have shown that reproductive success is lower when genetic similarity between parents is high, and that survival and other measures of fitness increase with individual levels of genetic diversity. These studies indicate that natural selection may favour the avoidance of matings with genetically similar individuals. But constraints on social mate choice, such as a lack of alternatives, can lead to pairing with genetically similar mates. In such cases, it has been suggested that females may seek extra-pair copulations with less related males, but the evidence is weak or lacking. Here we report a strong positive relationship between the genetic similarity of social pair members and the occurrence of extra-pair paternity and maternity ('quasi-parasitism') in three species of shorebirds. We propose that extra-pair parentage may represent adaptive behavioural strategies to avoid the negative effects of pairing with a genetically similar mate.

Multiple receivers, multiple ornaments, and a trade-off between agonistic and epigamic signaling in a widowbird.

Sexual displays often involve several different ornamental traits. Yet most indicator models of sexual selection based on a single receiver (usually a choosy female) find that multiple handicap signals should be unstable. Here we study reasons for this contradiction, analyzing signal function, signal content, and trade-offs between signals in the polygynous red-collared widowbird Euplectes ardens. Males have both a long, graduated tail and a red carotenoid collar badge. Territory-holding "residents" have slightly shorter tails than the nonbreeding "floaters," but their carotenoid collars are 40% larger, and they have (on the basis of reflectance spectrometry and objective colorimetry) a 23-nm more long-wave ("redder") hue than floaters. This corroborates experimental evidence that the red collar is selected by male contest competition, whereas female choice is based almost exclusively on male tail length. Tail length is negatively correlated with the carotenoid signal, which together with body size and condition explains 55% of the variation in tail length. The trade-off in tail length and carotenoid investment is steeper among residents, suggesting an interaction with costs of territory defense. We propose that the "multiple receiver hypothesis" can explain the coexistence of multiple handicap signals. Furthermore, the trade-off between signal expressions might contribute to the inverse relation between nuptial tail elongation and coloration in the genus Euplectes (bishops and widowbirds).

Clutch size limitation in waders: experimental test in redshank Tringa totanus.

Several hypotheses have been raised to explain the upper limit of clutch size at four eggs in waders (suborder Charadrii), which may play an important role in the evolution of the variety of mating and parental care systems in this group. Experimental tests of the hypotheses have produced conflicting results. It was recently suggested that the combined effects of several incubation costs of a larger clutch suffice to limit its size to four eggs in this group. Here we test the incubation-limitation hypothesis in a field experiment, in redshank Tringa totanus. We created five-egg clutches by adding one egg from another nest to a just completed four-egg clutch. Four-egg control clutches were created by replacing one of the eggs by an egg from another nest. All egg removals, additions and replacements were done before incubation started. Incubation time in five-egg clutches increased by 1 day to 24.3±0.23 days, compared to 23.3±0.32 days in four-egg clutches. Egg hatchability and nest predation rates did not differ significantly between treatments. On average five-egg clutches produced one extra chick at hatching (4.5±0.26 chicks) compared to four-egg clutches (3.5±0.27 chicks). Also when several additional costs from incubating enlarged clutches are added, redshanks by laying a fifth egg would on average increase their reproductive success at hatching by an estimated 22%. The incubation-limitation hypothesis therefore is clearly rejected in this species. Possible mechanisms behind the four-egg clutch limit in waders and ways of testing the alternatives are discussed.

EVOLUTION OF CONDITION-DEPENDENT SEX ORNAMENTS AND MATING PREFERENCES: SEXUAL SELECTION BASED ON VIABILITY DIFFERENCES.

The possibility that the evolution of mating preferences and secondary sex traits can be based on heritable differences in viability is examined with a three-locus model. Earlier genetic models suggested that viability-based processes alone cannot explain the evolution of mate choice and sex ornaments that reduce survival; a Fisherian mating advantage seemed necessary. The present model is based on a monogamous mating system that precludes such a mating advantage. A key assumption is that ornament development depends on the phenotypic condition and overall genotype of the possessor; there is evidence that secondary sex traits often mirror nutritional status and health, sometimes through hormonal mediation. Ornament and preference can then hitchhike slowly to high frequency with alleles that confer a slight survival advantage, provided that such alleles become available often enough. The evolution of mating preferences and secondary sex traits that reflect overall genotypic constitution therefore can be based solely on viability differences, no Fisherian mating advantage being required. In practice, these and several other mechanisms of sexual selection may occur together.