Rapid evolution of a sexually selected trait following population establishment in a novel habitat

Colonization of novel environments creates new selection pressures. Sexually selected traits are affected by the physical and social environment and should be especially susceptible to change, but this has rarely been studied. In southern California, dark-eyed juncos, (Junco hyemalis) naturally breed in mixed-coniferous temperate forests, typically from 1500 m to 3000 m in elevation. In the early 1980s, a small population became established in a coastal habitat, the University of California, San Diego campus, which has a mild, Mediterranean climate. I show that a sexually and socially selected signaling trait--the amount of white in the tail--has declined by approximately 22% as compared to mountain juncos. I address three main factors that could explain the difference between mountain and coastal juncos: phenotypic plasticity, genetic drift, and selection. Results indicate that the first two can be ruled out as the sole cause of the plumage change, which implies that selection contributed to the genetic differentiation from the mountain population. The estimated rate of evolution is about 0.2 haldanes, comparable with rates of change in systems where individuals have been artificially introduced into new environments (e.g., guppies and Drosophila). This is the first study to demonstrate evolution of a sexually selected trait after only several generations resulting from a natural invasion into a novel environment.     

Phenotypic plasticity and the evolution of a socially selected trait following colonization of a novel environment

Novel selection pressures in new environments arise through two distinct processes. First, environmental conditions directly affect the fitness of different phenotypes. Second, phenotypic plasticity alters the distribution of phenotypes, thereby placing populations in new selective regimes. A small isolated population of dark-eyed juncos Junco hyemalis became established in San Diego, probably in the early 1980s and probably from the nearby mountains. The relatively mild coastal climate has resulted in an increase in both the mean and the variance of the length of time females breed each year, and this is assumed to be a result of phenotypic plasticity. The population has evolved reduced white in the tail. We studied contemporary patterns of selection on tail white, in the context of the altered breeding season length. Late-hatched nestlings had higher survival and were in better condition than early-hatched nestlings, but among survivors, late-hatched birds had less tail white. We suggest this reflects juvenile mortality favoring individuals with less tail white. In adults, we found weak sexual selection and no viability selection but positive selection on female tail white in association with fecundity. We argue that altered breeding season length had a major impact on patterns of selection and evolution in this population.     

Early‐breeding females experience greater telomere loss

Annual reproductive success is often highest in individuals that initiate breeding early, yet relatively few individuals start breeding during this apparently optimal time. This suggests that individuals, particularly females who ultimately dictate when offspring are born, incur costs by initiating reproduction early in the season. We hypothesized that increases in the ageing rate of somatic cells may be one such cost. Telomeres, the repetitive DNA sequences on the ends of chromosomes, may be good proxies of biological wear and tear as they shorten with age and in response to stress. Using historical data from a long‐term study population of dark‐eyed juncos (Junco hyemalis), we found that telomere loss between years was greater in earlier breeding females, regardless of chronological age. There was no relationship between telomere loss and the annual number of eggs laid or chicks that reached independence. However, telomere loss was greater when temperatures were cooler, and cooler temperatures generally occur early in the season. This suggests that environmental conditions could be the primary cause of accelerated telomere loss in early breeders.     

Steroid hormones and immune function: experimental studies in wild and captive dark-eyed juncos (Junco hyemalis)

Monogamous and polygynous male songbirds generally differ in their breeding season profiles of circulating testosterone. Testosterone level spikes early in the breeding season of monogamists and then declines, but it remains high in polygynists. Male dark-eyed juncos (Junco hyemalis) are socially monogamous and exhibit the usual pattern, but experimental maintenance of high testosterone throughout the breeding season alters normal behavior and physiology and affects various components of annual reproductive success but not overall annual success. Because stabilizing selection predicts that alteration of naturally existing phenotypes should reduce lifetime reproductive success, we asked whether prolonged testosterone exposure might impair immune function and perhaps thereby reduce life span. We assessed immune function in captive and wild male juncos that we treated with either testosterone-filled or empty Silastic implants. Results indicate that prolonged elevation of testosterone suppresses antibody production in captive males and cell-mediated immunity in wild males. Together these results suggest that testosterone-treated males may be more susceptible to disease or parasitic infection. As earlier studies have shown, levels of corticosterone as well as testosterone are higher in testosterone-treated males, so it is unclear whether the immune suppression we observed is due to testosterone's direct effects on immunity or testosterone's influence on glucocorticoid production. We discuss results in the context of recent hypotheses regarding life-history theory and potential endocrine-immune interactions.     

Reduced immunocompetence of nestlings in replacement clutches of the European magpie (Pica pica)

Laying date is one of the most important determinants of reproductive success and recruitment probability in birds. Late breeders usually fledge fewer chicks than individuals with earlier breeding dates, and fledglings produced late in the season have high mortality rates. Food availability and nestling mass have been evoked as the principal mechanistic links between laying date and offspring survival. Here we suggest that another factor may actually account for the difference in survival rate between early and late offspring: immunocompetence. We predicted that nestlings produced later in the season or in replacement clutches should have lower immune responses when challenged with an antigen, than early nestlings or nestlings produced in first clutches. This hypothesis was tested in a population of magpies (Pica pica), in which we experimentally induced breeding failure in a group of nests and compared the immune response of nestlings in replacement clutches with the immune response of first clutch nestlings. Cellular immune response, as measured by wing web swelling (a correlate of T-lymphocyte production after injection of phytohaemagglutinin-P), significantly decreased with hatching date and was significantly lower in nestlings of replacement clutches. Furthermore, coefficients of intraclutch variation in immune response were higher in nestlings of replacement clutches. This experiment demonstrates an inverse relationship between immune responsiveness and breeding date, and reduced recruitment probability of late nestlings may be a direct consequence of their inability to cope with parasites.     

Human-resource subsidies alter the dietary preferences of a mammalian top predator

Seasonal fitness declines are common, but the relative contribution of different reproductive components to the seasonal change in the production of reproductive young, and the component-specific drivers of this change is generally poorly known. We used long-term data (17 years) on breeding time (i.e. date of first egg laid) in northern wheatears (Oenanthe oenanthe) to investigate seasonal reproductive patterns and estimate the relative contributions of reproductive components to the overall decline in reproduction, while accounting for factors potentially linked to seasonal declines, i.e. individual and habitat quality. All reproductive components—nest success (reflecting nest predation rate), clutch size, fledging success and recruitment success—showed a clear decline with breeding time whereas subsequent adult survival did not. A non-linear increase in nest predation rate caused nest success to decline rapidly early in the season and level off at ~80 % success late in the breeding season. The combined seasonal decline in all reproductive components caused the mean production of recruits per nest to drop from around 0.7–0.2; with the relative contribution greatest for recruitment success which accounted for ~50 % of the decline. Our data suggest that changing environmental conditions together with effects of nest predation have strong effects on the seasonal decline in fitness. Our demonstration of the combined effects of all reproductive components and their relative contribution shows that omitting data from later stages of breeding (recruitment) can greatly underestimate seasonal fitness declines.     

Rainfall during parental care reduces reproductive and survival components of fitness in a passerine bird

Adverse weather conditions during parental care may have direct consequences for offspring production, but longer‐term effects on juvenile and parental survival are less well known. We used long‐term data on reproductive output, recruitment, and parental survival in northern wheatears (Oenanthe oenanthe) to investigate the effects of rainfall during parental care on fledging success, recruitment success (juvenile survival), and parental survival, and how these effects related to nestling age, breeding time, habitat quality, and parental nest visitation rates. While accounting for effects of temperature, fledging success was negatively related to rainfall (days > 10 mm) in the second half of the nestling period, with the magnitude of this effect being greater for breeding attempts early in the season. Recruitment success was, however, more sensitive to the number of rain days in the first half of the nestling period. Rainfall effects on parental survival differed between the sexes; males were more sensitive to rain during the nestling period than females. We demonstrate a probable mechanism driving the rainfall effects on reproductive output: Parental nest visitation rates decline with increasing amounts of daily rainfall, with this effect becoming stronger after consecutive rain days. Our study shows that rain during the nestling stage not only relates to fledging success but also has longer‐term effects on recruitment and subsequent parental survival. Thus, if we want to understand or predict population responses to future climate change, we need to consider the potential impacts of changing rainfall patterns in addition to temperature, and how these will affect target species' vital rates.     

The adaptive value of energy storage and capital breeding in seasonal environments

Timing of reproduction in a seasonal cycle is a life history trait with important fitness consequences. Capital breeders produce offspring from stored resources and, by decoupling feeding and reproduction, may bend the constraints caused by seasonality in food or predation. Income breeders, on the other hand, produce offspring from concurrent food intake, with the disadvantage of less flexibility, but with high efficiency and no inventory costs of carrying stores. Here, we assess relative profitability of capital and income breeding in herbivorous zooplankton inhabiting seasonal, high-latitude environments. We apply a state-dependent life history model where reproductive values are used to optimise energy allocation and diapause strategies over the year. Three environmental scenarios were modelled: an early, an intermediate, and a late feeding season. We found that capital breeding was most important in the early season. Capital breeding ranged from 7–9% of the eggs produced but, because of the high reproductive value of early eggs, capital breeding ranged from 9–30% when measured in terms of reproductive value. The main benefit of capital breeding was reproduction prior to the feeding season – when the reproductive value of an egg peaked. In addition, capital breeding was also used to increase egg production rates at times of income breeding. For individuals born late in the season the model predicted a two-year cycle instead of the typical annual life cycle. These individuals could then reap the benefits of early reproduction and capital breeding in their second year instead of income breeding late in the first year. We emphasize the importance of evaluating reproductive strategies such as capital and income breeding from a complete life cycle perspective. In particular, knowing the seasonality in offspring fitness is essential to appreciate evolutionary and population-level consequences of capital breeding.     

Selection for synchronous breeding in the European starling

Colonial birds often demonstrate considerable breeding synchrony. In southern Sweden the semi-colonial European starling initiated the vast majority of clutches within one week. Laying dates were positively skewed so that many birds initiated clutches at similar dates early in the season. Breeding was further synchronised by a particularly strong clutch-size reduction equivalent to one third of an egg per day during the first part of the breeding season. The decline in clutch size with season also held true for separate age-classes of females, for individual females laying at different times at different years and for individual females laying at different times the same year. Trends in breeding success during nestling rearing were unlikely to explain the high degree of breeding synchrony or the seasonal decline in clutch size; nestling survival and growth were weakly related or unrelated to reproductive timing. In contrast recruitment success of fledged offspring declined sharply with season. Even within the synchronous laying period, defined as clutches initiated during the first week each year, local recruitment success declined. It is suggested that the early seasonal decline is caused by selection for synchronous fledging permitting the immediate formation of flocks after fledging, whereas the late seasonal trends may be caused by either population differences in female quality or deteriorating conditions for raising young.     

The early‐life environment and individual plasticity in life‐history traits

We tested whether the early‐life environment can influence the extent of individual plasticity in a life‐history trait. We asked: can the early‐life environment explain why, in response to the same adult environmental cue, some individuals invest more than others in current reproduction? Moreover, can it additionally explain why investment in current reproduction trades off against survival in some individuals, but is positively correlated with survival in others? We addressed these questions using the burying beetle, which breeds on small carcasses and sometimes carries phoretic mites. These mites breed alongside the beetle, on the same resource, and are a key component of the beetle's early‐life environment. We exposed female beetles to mites twice during their lives: during their development as larvae and again as adults during their first reproductive event. We measured investment in current reproduction by quantifying average larval mass and recorded the female's life span after breeding to quantify survival. We found no effect of either developing or breeding alongside mites on female reproductive investment, nor on her life span, nor did developing alongside mites influence her size. In post hoc analyses, where we considered the effect of mite number (rather than their mere presence/absence) during the female's adult breeding event, we found that females invested more in current reproduction when exposed to greater mite densities during reproduction, but only if they had been exposed to mites during development as well. Otherwise, they invested less in larvae at greater mite densities. Furthermore, females that had developed with mites exhibited a trade‐off between investment in current reproduction and future survival, whereas these traits were positively correlated in females that had developed without mites. The early‐life environment thus generates individual variation in life‐history plasticity. We discuss whether this is because mites influence the resources available to developing young or serve as important environmental cues.     

Experience versus effort: what explains dynamic heterogeneity with respect to age?

Age‐related patterns of survival and reproduction have been explained by accumulated experience (‘experience hypothesis’), increased effort (‘effort hypothesis’), and intrinsic differences in phenotypes (‘selection hypothesis’). We examined the experience and effort hypotheses using a 40‐year data set in a population of Leach's storm‐petrels Oceanodroma leucorhoa, long‐lived seabirds for which the effect of phenotypic variation has been previously demonstrated. Age was quantified by time since recruitment (‘breeding age’). The best model of adult survival included a positive effect of breeding age (1, 2, 3+ years), sex (male > female), and year. Among‐individuals variation (fixed heterogeneity) accounted for 31.6% of the variance in annual reproductive success. We further examined within‐individual patterns in reproductive success (dynamic heterogeneity) in the subset of individuals with at least five breeding attempts. Three distinct phases characterized reproductive success – early increase, long asymptotic peak, late decline. No effect of early reproductive output on longevity was found, however, early success was positively correlated with lifetime reproductive success. Reproductive success was lower earlier than later in life. Among the few natally philopatric individuals in the population, age of first breeding had no effect on longevity, lifetime reproductive success, or early reproductive success. No support for the effort hypothesis was found in this population. Instead, age‐specific patterns of survival and reproduction in these birds are best explained by the experience hypothesis over and above the effect of intrinsic differences among individuals.     

Experimental evidence that age-specific reproductive success is independent of environmental effects

An age-specific improvement in reproductive performance has been reported in many iteroparous breeders. However, whether this is a consequence of intrinsic differences in competence amongst age classes or extrinsic differences in the environment they experience is unclear since the timing of breeding within a season generally also differs with age. To disentangle these effects, we experimentally manipulated the timing of breeding in shags, Phalacrocorax aristotelis. Old and young individuals thus reared their chicks at the same time both early and late in the breeding season. When breeding in the same environmental conditions, old pairs performed consistently better than young pairs. These data clearly demonstrate that the age-related differences in reproductive performance are not a result of environmental effects, but rather a consequence of intrinsic differences in brood rearing capacity.     

Double brooding and offspring desertion in the barn owl Tyto alba

Many bird species produce two annual broods during a single breeding season. However, not all individuals reproduce twice in the same year suggesting that double brooding is condition‐dependent. In contrast to most raptors and owls, the barn owl Tyto alba produces two annual clutches in most worldwide distributed populations. Nevertheless, the determinants of double brooding are still poorly studied. We performed such a study in a Swiss barn owl population monitored between 1990 and 2014. The annual frequency of double brooding varied from 0 to 14% for males and 0 to 59% for females. The likelihood of double brooding was higher when individuals initiated their first clutch early rather than late in the season and when males had few rather than many offspring at the first nest. Despite the reproductive benefits of double brooding (single‐ and double‐brooded individuals produced 3.97 ± 0.11 and 7.07 ± 0.24 fledglings, respectively), double brooding appears to be traded off against offspring quality because at the first nest double‐brooded males produced poorer quality offspring than single‐brooded males. This might explain why females desert their first mate to produce a second brood with another male without jeopardizing reproductive success at the first nest. Furthermore, the reproductive cycle being very long in the barn owl (120 d from start of laying to offspring independence), selection may have favoured behaviours that accelerate the initiation of a second annual brood. Accordingly, half of the double‐brooded females abandoned their young offspring to look for a new partner in order to initiate the second breeding attempt, 9.48 d earlier than when producing the second brood with the same partner. We conclude that male and female barn owls adopt different reproductive strategies. Females have more opportunities to reproduce twice in a single season than males because mothers are not strictly required during the entire rearing period in contrast to fathers. A high proportion of male floaters may also encourage females to desert their first brood to re‐nest with a new male who is free of parental care duties.     

The reproductive strategy of Leporinus friderici (Characiformes, Anostomidae) in the Paraná River basin: the effect of reservoirs

The reproductive strategy of a species depends upon the interaction between intrinsic and extrinsic factors. Examining the population of Leporinus friderici in two reservoirs of the Upper Paraná River basin in reference to first gonadal maturation and breeding season and sites, the present investigation tested whether the environment formed by damming promoted spatial and temporal changes in the reproductive strategy of this species. Analyses of sex ratios showed that females significantly predominated in Itaipu, while in Corumbá the sexes were about equal with a slight predominance of males. Size-associated sexual dimorphism was observed, that is females dominated the longer length categories, and males the shorter. The minimum size at which L. friderici initiated reproduction varied from year to year, and was larger in the periods soon after formation of both reservoirs. In Itaipu, stabilization between the maximum and minimum lengths at first maturation was also noted after year 6 following closure and continuing until year 15. In general, the breeding season lasted from October through April, although cyclic changes in the duration and intensity of this season were evident. Young individuals predominated during the entire study period in Corumbá. The formation of Itaipu Reservoir had a greater effect on the reproduction of L. friderici, where a gradual adaptation of the reproductive strategy of this species may possibly have been occurring. It is also possible that some of the characteristics of the Itaipu population will in the future be shown by the Corumbá population. It was concluded that reproductive strategies constitute ecological adaptations that are temporally and spatially altered and are fitted to resource availability and environmental pressure.     

Information thresholds,habitat loss and population persistence in breeding birds

The combination of spatial structure and non‐linear population dynamics can promote the persistence of coupled populations, even when the average population growth rate of the patches seen in isolation would predict otherwise. This phenomenon has generally been conceptualized and investigated through the movement of individuals among patches that each holds many individuals, as in metapopulation models. However, population persistence can likewise increase as the result of individuals moving among sites (e.g. breeding territories) within in a single patch. Here I examine the latter: individuals making small‐scale informed decisions with respect to where to breed can promote population persistence in poor environments. Based on a simple algebraic model, I demonstrate information thresholds, and predict that greater information use is required for population persistence under lower spatial heterogeneity in habitat quality, all else equal. Second, I implement an individual‐based model to explore prior experience and prospecting on conspecific success within a more complex, and spatially heterogeneous environment. Uniquely, I jointly examine the effects of simulated habitat loss, spatial heterogeneity prior to habitat, and variation in information gathering on population persistence. I find that habitat loss accelerates population quasi‐extinction risk; however, information use reduces extinction probabilities in proportion to the level of information gathering. Per capita reproductive success declines with number of breeding sites, suggesting that information‐mediated Allee effects may contribute to extinction risk. In conclusion, my study suggests that populations in a changing world may be increasingly vulnerable to extinction where patch size and spatial heterogeneity constrain the effectiveness of information‐use strategies.     

Local breeding experience and the reproductive performance of Tree Swallows

ABSTRACT The potential advantages of repeated breeding at a particular location should improve reproductive performance in long‐lived species of birds. However, for short‐lived species, natural selection should favor individuals that most quickly develop competency in reproduction. Therefore, we hypothesized that local breeding experience beyond the first breeding attempt at a particular location would have little effect on subsequent reproductive performance of Tree Swallows (Tachycineta bicolor), a species where about 50% of adults breed only once in their lives. We tested this hypothesis using data collected from Tree Swallows in Michigan from 1993 to 2002. Because we were specifically interested in examining the effects of local breeding experience on reproductive performance, we restricted our analyses to after‐second‐year (ASY) females and their mates that we first encountered as breeders. Consistent with our hypothesis, we found no relationship between repeated local breeding experience and the reproductive performance of ASY female Tree Swallows and their mates as measured by clutch size and number of fledged young. However, pairs with more combined total local experience tended to lay eggs earlier in the season. These results suggest that Tree Swallows may benefit from breeding site fidelity, not because repeated local experience improves reproductive performance as measured by the production of fledglings, but because returning individuals acquire nest cavities earlier and are able to begin breeding earlier, providing time to renest in case of early nest failure.     

Sexual maturity increases mobility and heterogeneity in individual space use in Atlantic salmon (Salmo salar) parr

We assessed the effects of sexual maturity on space use in Atlantic salmon (Salmo salar) parr as facultative early maturation enables us to work on individuals belonging to the same cohort. We monitored the space use of 40 1-year-old males in natura throughout a breeding season. First, mature individuals covered longer distances (absolute and upstream) and located within broader home ranges than immature parr. Second, sexual maturity also generated a higher interindividual variability in space use. Finally, mature individuals exhibited a higher probability of association with likely breeding sites on average. However, some mature individuals experienced a lower probability than immature individuals, suggesting that the space use of some mature individuals may not be optimal. Moreover, mature parr exploiting a broader home range or covering longer upstream distances had a higher probability of association with likely breeding sites. Covering longer upstream distances may therefore increase the reproductive success of mature parr, while involving higher energetic costs and a greater risk of predation.     

Life history of the ghost shrimp, Callianassa japonica Ortmann (Decapoda: Thalassinidea), on an intertidal sandflat in western Kyushu, Japan

Growth, density, survival, and reproduction were examined for the population of the ghost shrimp, Callianassa japonica Ortmann, inhabiting an intertidal sandflat in western Kyushu, Japan, based on samples collected from May, 1989 to April, 1991. During the breeding season (June–October) each year, there were two discrete periods of egg production by females. The post-larval settlement, with a time-lag of 1–1.5 months (brooding plus larval developmental periods), generated two major recruitment cohorts, occurring in July–August (1st cohort) and September–November (2nd cohort). The higher growth rate of individuals after recruitment in the 1st cohort enhanced the separation of the two cohorts. Between sexes, the subsequent life history patterns and population characteristics were, for the most part, similar. In females, the majority of individuals of each of the two cohorts matured after approximately one year, respectively, at around a 20-mm total body length, and a portion of these cohorts survived as a fused cohort until June of the second year, breeding again prior to dying off by the end of September. The pattern of growth was an indeterminate type. For each of the two cohorts, the growth rates changed at two transition points of their life history, at around the beginning of their two breeding seasons. The growth rate for the 1st cohort slowed down at the first transition point, while that for the 2nd cohort speeded up there. This led to the approach and fusion of the two cohorts near the second transition point, when growth stopped. During periods other than the breeding seasons, high survival rates were exhibited by the two cohorts. During the first breeding season, a significantly low survival rate was observed for the 1st cohort, but not for the 2nd cohort. The degree of participation in breeding activity may be responsible for the above differences between cohorts. In the two male cohorts, while the cost of reproduction did not reduce the growth rates during the first breeding season, it lowered their survival rates more severely compared to those of females. This may be responsible for the slightly female-biased sex ratio in the population (1.06:1). The density of the population as a whole was stable throughout the study period, with the mean ± SD being 901 ± 157/m² (n = 27); the adult population declines during the breeding seasons were effectively replenished by recruitment each year.     

Females competing to reproduce: dominance matters but testosterone may not

The associations among aggression, testosterone (T), and reproductive success have been well studied, particularly in male birds. In many species, males challenged with simulated or real territorial intrusions increase T and levels of aggression, outcomes linked to higher dominance status and greater reproductive success. For females, the patterns are less clear. Females behave aggressively towards one another, and in some species, females respond to a social challenge with increases in T, but in other species they do not. Prior work on female dark-eyed juncos (Junco hyemalis) had shown that experimental elevation of T increases social status and intrasexual aggression. Here, we conducted two experiments designed to answer three questions: Are endogenous concentrations of T associated with dominance status in captive female juncos? Does dominance status influence readiness to breed in female juncos? And do captive females increase T in response to a challenge? In the first experiment, we introduced two females to a breeding aviary, allowed them to form a dominance relationship and then introduced a male. We found that dominant females were more likely to breed than subordinates, but that dominance status was not predicted by circulating T. In the second experiment, we allowed a resident male and female to establish ownership of a breeding aviary (territory) then introduced a second, intruder female. We found that resident females were aggressive towards and dominant over intruders, but T did not increase during aggressive interactions. We suggest that during the breeding season, intrasexual aggression between females may influence reproductive success, but not be dependent upon fluctuations in T. Selection may have favored independence of aggression from T because high concentrations of T could interfere with normal ovulation or produce detrimental maternal effects.     

Syphacia obvelata infections and reproduction of male domestic mice Mus musculus domesticus on a sub-Antarctic Island

The reproductive activity of feral male mice on an island of the sub-Antarctic Kerguelen archipelago was influenced by biological factors depending on periods within the breeding season. After having controlled host reproductive activity indices for body size, i.e. age, and body condition effects, Syphacia obvelata prevalence did not vary with host reproductive status or age either during the beginning or the middle-end of the reproductive season. Considering the beginning of the breeding season, worm abundance was more pronounced in males the year following a strong winter crash of the population than in years when high over wintering survival occurred. During the middle-end of the breeding season, males with the highest reproductive status were more infected than males with a lower reproductive status in years when oldest individuals dominated the population. It is suggested that this situation was due to an endocrine related increased host susceptibility partly influenced by a change in the age structure of the population, and that an increase in worm transmission was not directly related to male activity concurrent with reproductive status, nor to population density.