Protandry and sexual dimorphism in trans-Saharan migratory birds

Earlier arrival to reproductive sites of males relative to females(protandry) is widespread among migratory organisms. Diversemechanisms have been proposed that may select for protandry,including competition for limiting resources (e.g., territories)or mates. In species with large variation in male reproductivesuccess, such as polygamous species and those with intense spermcompetition, early arriving males may accrue a fitness advantagebecause they acquire more mates or have larger chances of paternity.Comparative studies of birds have shown that sexual size dimorphism(SSD) is positively associated with the level of polygyny, whereasintense sperm competition is associated with sexual dichromatism(SD). Positive correlations between protandry and SSD or SDcan therefore be expected to exist across avian species. Becauselarge males are predicted to be better able to cope with adverseecological conditions early in the breeding season, selectionfor protandry, in turn, may have a correlated response on SSDamong migratory species breeding in boreal latitudes. Althoughprevious studies of birds have analyzed the association betweenSSD and protandry, none has analyzed SD in relation to protandry.Here we analyze the association between protandry during springmigration, SSD, and SD in 21 trans-Saharan monogamous migratorybird species. The difference in median migration dates betweenfemales and males, reflecting protandry, was positively associatedwith SD but not with SSD. Because dichromatism is positivelyrelated to sperm competition across species, present resultsare consistent with predictions derived from sexual selectionhypotheses for the evolution of protandry mediated by spermcompetition.     

Why do female migratory birds arrive later than males?

1. In migratory birds males tend to arrive first on breeding grounds, except in sex-role reversed species. The two most common explanations are the rank advantage hypothesis, in which male-male competition for breeding sites drives stronger selection for early arrival in males than females, and the mate opportunity hypothesis, which relies on sexual selection, as early arrival improves prospects of mate acquisition more for males than for females. 2. To date, theoretical work has focused on selection for early arrival within a single sex, usually male. However, if fitness depends on territory quality, selection for early arrival should operate on both sexes. Here we use two independent modelling approaches to explore the evolution of protandry (male-first arrival) and protogyny (female-first arrival) under the rank advantage and mate opportunity hypotheses. 3. The rank advantage hypothesis, when operating alone, fails to produce consistent patterns of protandry, despite our assumption that males must occupy territories before females. This is because an individual of either sex benefits if it out-competes same-sex competitors. Rather than promoting protandry, the rank advantage mechanism can sometimes result in protogyny. Female-female competition is stronger than male-male competition early in the season, if females compete for a resource (territories occupied by males) that is initially less common than the resource of interest to males (unoccupied territories). 4. Our results support the mate opportunity hypothesis as an explanation of why protandry is the norm in migratory systems. Male-biased adult sex ratios and high levels of sperm competition (modelled as extra-pair young: EPY) both produce protandry as a result of sexual selection. Protogyny is only observed in our models with female-biased sex ratios and low EPY production. 5. We also show that the effects of sex ratio biases are much stronger than those of EPY production, explore the evidence for sex ratio biases and extra-pair paternity in migratory species and suggest future research directions.     

Migration phenology and winter habitat quality are related to circulating androgen in a long‐distance migratory bird

In migratory birds, the timing of departure from wintering grounds is often dependant on the quality of habitat on an individual's territory and may influence individual fitness, resulting in an interaction of life history stages across large geographical distances. American redstart Setophaga ruticilla males who overwinter in high quality habitats arrive early to breed and subsequently produce more offspring than late arrivers. Since many migratory species overlap vernal migration with the physiological transition to breeding, we examined if breeding preparation plays a role in this seasonal interaction. We tested the hypothesis that early arriving male redstarts from high quality winter habitats are in superior breeding condition by simultaneously measuring winter habitat quality (stable‐carbon isotopes) and breeding preparation (circulating androgen, cloacal protuberance (CP) diameter) upon arrival at breeding grounds. Compared with late arrivers, early arriving males were from higher quality winter habitats and had higher androgen, but smaller CPs. Males arriving with higher androgen were in more advanced physiological migratory condition, as measured by haematocrit. Early arrivers were more likely to successfully breed, but there was no significant relationship between androgen upon arrival and breeding success. One possible explanation for these relationships is that androgen measured during arrival is most relevant in a migratory context, such that birds with high androgen may benefit from effects on migratory condition, positively influencing fitness through earlier arrival.     

Spatial Isolation and Temporal Variation in Fitness and Condition Facilitate Divergence in a Migratory Divide

A novel migratory polymorphism evolved within the last 60 years in blackcaps (Sylvia atricapilla) breeding sympatrically in southwestern Germany. While most individuals winter in the traditional areas in the Mediterranean, a growing number of blackcaps started migrating to Britain instead. The rapid microevolution of this new strategy has been attributed to assortative mating and better physical condition of birds wintering in Britain. However, the isolating barriers as well as the physical condition of birds are not well known. In our study, we examined whether spatial isolation occurred among individuals with distinct migratory behaviour and birds with different arrival dates also differed in physical and genetic condition. We caught blackcaps in six consecutive years upon arrival on the breeding grounds and assigned them via stable isotope analysis to their wintering areas. Analysis of the vegetation structure within blackcap territories revealed different microhabitat preferences of birds migrating to distinct wintering areas. Blackcaps arriving early on the breeding grounds had higher survival rates, better body condition and higher multilocus heterozygosities than later arriving birds. We did however not find an effect of parasite infection status on arrival time. Our results suggest that early arriving birds have disproportionate effects on population dynamics. Allochrony and habitat isolation may thus act together to facilitate ongoing divergence in hybrid zones, and migratory divides in particular.     

Absence of protandry in the spring migration of a population of Song Sparrows Melospiza melodia

Early male arrival at breeding sites, or protandry, is thought to have evolved from intrasexual competition among males for access to mates or breeding resources. Males of polygynous species tend to be larger than females and have exaggerated secondary sexual traits. Additionally, such species show a high degree of protandry, suggesting that timing of arrival is sexually selected. Species showing limited sexual dimorphism and showing sexual monochromatism may be expected to show limited early male arrival. However, there are very few studies of migration timing of the sexes in such species because individuals cannot be readily identified to sex in the hand. In this study, we genetically sexed birds and found no evidence for early male arrival, for a population of migratory Song Sparrows Melospiza melodia . For our study population, males and females display limited sexual size dimorphism and are sexually monochromatic which is characteristic of the species. Fat scores for males were inversely associated with timing of arrival, whereas for females, larger-winged birds arrived sooner – suggesting that early migration timing may be selected for in both sexes.     

Size-dependent selection on arrival times in sticklebacks: why small males arrive first

Abstract Studies on arrival time to breeding areas show that high-quality males usually arrive first and gain the highest reproductive success. This is generally assumed to be due to phenotype-dependent costs and benefits of early arrival. We show that the opposite arrival order can occur, probably due to selection on poor-quality males to increase their chances of reproduction. In a fish species, the threespine stickleback, Gasterosteus aculeatus , small males arrived before larger males at the breeding grounds. Early arrival was costly because predation risk was at its highest at the start of the season and early territory establishment was selected against, as demonstrated by selection coefficients for territory maintenance and hatching success. Large males probably postponed arrival until females were available to decrease predation risk costs and increase offspring production. An experimental study showed that a delay in arrival of large males does not decrease their probability of reproduction, because large males are able to take over nest sites from small males. Small males, on the other hand, are less likely to establish territories in competition with large males but can pay the costs of early arrival in exchange for the benefit of access to territories. Thus, whereas natural selection favors later arrival, sexual selection through competition for breeding territories favors early arrival in small, competitively inferior males. This results in the benefits of early arrival depending on the competitive ability of the male, which favors size-dependent optimal arrival times.     

Relationship between arrival timing and breeding success of intra‐tropical migratory Fork‐tailed Flycatchers (Tyrannus savana)

For migratory birds, early arrival at breeding areas has many benefits, such as acquisition of better territories and mates. This strategy has been found in numerous species breeding at north‐temperate latitudes, but has not been yet reported for intra‐tropical migratory species. We evaluated the relationship between arrival date, initiation of breeding, and breeding success of Fork‐tailed Flycatchers (Tyrannus savana) breeding in southeastern Brazil and overwintering in northern South America. We color‐banded adult flycatchers during three breeding seasons and searched for them during the following breeding seasons. We also monitored nests from construction until either failure or fledging of young. We found that: (1) male Fork‐tailed Flycatchers arrived at the breeding site earlier than females, (2) males that arrived earlier had greater breeding success, and (3) nests where eggs were laid earlier in the breeding season were more likely to be successful than those where eggs were laid later. Male Fork‐tailed Flycatchers appeared to benefit from early arrival at a tropical breeding site, potentially mediated by their ability to acquire a high‐quality territory and mate as early as possible, and by the ability of their mate to begin breeding as early as possible. Breeding success for female Fork‐tailed Flycatchers may be determined primarily by a combination of the arrival date of their mate and how quickly they can begin breeding. Our results suggest that protandry occurs in an intra‐tropical migratory bird and that early arrival of males and early initiation of reproduction by females results in greater reproductive success. A better understanding of the underlying mechanisms that control the timing of migration and reproduction of this and other intra‐tropical migratory species is important for evaluating the challenges they face in light of current and future rapid environmental changes.     

Carry‐over effects of winter habitat quality on en route timing and condition of a migratory passerine during spring migration

We examined how conditions prior to migration influenced migration performance of two breeding populations of black‐and‐white warblers Mniotilta varia by linking information on the migrant's winter habitat quality, measured via stable carbon isotopes, with information on their breeding destination, measured via stable hydrogen isotopes. The quality of winter habitat strongly influenced the timing of migration when we accounted for differential timing of migration between breeding populations. Among birds migrating to the same breeding destination, males and females arriving early to the stopover site originated from more mesic habitat than later arriving birds, suggesting that the benefits of occupying high‐quality mesic habitat during the winter positively influence the timing of migration. However, male warblers arriving early to the stopover site were not in better migratory condition than later arriving conspecifics that originated from poor‐quality xeric winter habitat, regardless of breeding destination. The two breeding populations stopover at the study site during different time periods, suggesting that the lower migratory condition of early birds is not a function of the time of season, but potentially a migrant's migration strategy. Strong selection pressures to arrive early on the breeding grounds to secure high‐quality breeding territories may drive males from high‐quality winter habitat to minimize time at the expense of energy. This migration strategy would result in a smaller margin of safety to buffer the effects of adverse weather or scarcity of food, increasing the risk of mortality. The migratory condition of females was the same regardless of the timing of migration or breeding destination, suggesting that females adopt a strategy that conserves energy during migration. This study fills an important gap in our understanding of the linkages between winter habitat quality and factors that influence the performance of migration, the phase of the annual cycle thought to be limiting most migratory bird populations.     

Fat stores of American redstarts Setophaga ruticilla arriving at northerly breeding grounds

Many long-distance passerine migrants arrive with more fat stores than necessary to have reached their northerly breeding grounds. Researchers have argued for adaptive advantages associated with arriving with 'surplus' migratory fat, including increased breeding performance and insurance against adverse weather, and reduced food resources during the days following arrival. The objectives of this work were to document fat stores in American redstarts Setophaga ruticilla arriving to breed in northern Michigan and to test predictions associated with the hypothesis that arrival fat serves an insurance role. Results suggest that redstarts arrived in northern Michigan with fat stores sufficient to have continued migrating an additional distance greater than 1000 km. Significant yearly variation in arrival fat corresponded in part with environmental conditions measured at the breeding grounds. Birds arrived with the most fat in the year with the coolest temperatures and the lowest food abundance at the time of arrival to the site. Further, an inverse relationship between arrival fat and arrival day in males indicated that early arrivals carried more fat than later arrivals. Birds that arrived early faced cooler temperatures and lower densities of terrestrial invertebrates, and arrival fat may have provided a mechanism to overcome poor early season foraging conditions. However, our results are not entirely consistent with the hypothesis that arrival fat serves only as insurance. Arrival fat appeared important even during the most benign year of this study. Further, evidence suggests that females may have derived more benefit from arrival fat than males. These results highlight the connection between phases of a bird's annual cycle. Migrants that do well en route , arrive at breeding grounds in better condition, which may contribute to survival and reproductive success.     

Protandry, sexual selection and climate change

Protandry refers to the earlier appearance of males before females at sites of reproduction. Sexual selection has been hypothesized to give rise to sex differences in benefits and costs of early arrival, thereby selecting for earlier appearance by the sex subject to more intense sexual selection. If sexual selection is more intense, there is a greater premium on early arrival among individuals of the chosen sex because of direct selection for earlier arrival. This hypothesis leads to the prediction that changes in the costs and benefits of early arrival related to changes in environmental conditions should particularly affect the sex that arrives first and hence the degree of protandry. I tested this hypothesis using the Barn Swallow Hirundo rustica. During 1971–2003, the degree of protandry increased significantly in a Danish population because males advanced arrival date while females did not. This earlier arrival by males compared with females was correlated with a significant increase by over 1.2 standard deviations in the length of the outermost tail feathers of males, a secondary sexual character, suggesting direct selection on both protandry and the secondary sexual character. Environmental conditions during spring migration in Northern Africa, as reflected by the normalized difference vegetation index, have deteriorated since 1984, resulting in increased mortality among males during spring migration, but not among females, and this deterioration of climatic conditions was positively correlated with an increasing degree of protandry. Likewise, an increase in April temperatures at the breeding grounds during recent decades is positively correlated with increased protandry, apparently because males can arrive earlier without increasing the fitness cost of early arrival. Local population size did not predict changes in arrival date. These findings suggest that rapid changes in climate can cause a change in degree of protandry and secondary sexual characters.     

Degree of protandry reflects level of extrapair paternity in migratory songbirds

Males of most migratory organisms, including many birds, precede female conspecifics on their journey to the breeding areas. Several hypotheses have been proposed to explain the evolution of protandrous migration, yet they have rarely been tested at the interspecific level. Here, we provide correlational support for the “mate opportunity” hypothesis, which assumes that selection favours protandry in polygynous species where males gain significant fitness benefits from arriving earlier than females. Drawing on phenological data collected at two northern European stopover sites, we show that the time-lag in spring passage between males and females of five Palearctic migratory songbird species is positively associated with levels of extrapair paternity available from the literature. This suggests that males arrive relatively more in advance of females in species with high sperm competition where sexual selection through female choice is intense. Thus, protandry may arise from selection on the relative arrival timing of males and females rather than from selection within one of the sexes.     

Starting over: experimental effects of breeding delay on reproductive success in early‐arriving male American redstarts

Birds that arrive and breed early often have higher reproductive success than late individuals, either as a consequence of timing‐specific advantages (the timing hypothesis) or because these individuals and/or their resources are of higher quality (the quality hypothesis). In this study, we examined the potential influence of several factors affecting reproductive success by experimentally delaying breeding of early‐arriving male American redstarts Setophaga ruticilla, a species for which early male arrival is strongly related to increased reproductive success. Our manipulation involved the capture, holding, and release of males following pairing and territory establishment, resulting in the majority of subjects (67%) losing their initial mate (47%) or mate and territory (20%) and forcing them to start over approximately 12 d after their initial arrival. Males forced to start over (i.e. those losing their first territory and/or mate) did not experience any decrease in body condition, nor did their reproductive behaviour differ from that of early‐arriving control males. We found that naturally early‐arriving but experimentally manipulated males suffered reduced fledging success in comparison to early‐arriving males that bred early or late, but equivalent success in comparison to males that arrived and bred late. Based on our results, we propose that the relationship between early arrival and higher reproductive success in this species is mediated not simply by individual male quality or absolute arrival timing alone, but rather some other aspect of resource quality is likely important. We discuss and present evidence for two alternative explanations under the quality hypothesis: female quality and territory quality. To our knowledge, our study is the first to investigate the effects of experimentally delaying male breeding time, strengthening previous correlational evidence for resource quality as a potentially important selective agent driving early arrival in migratory birds.     

Plumage brightness predicts non-breeding season territory quality in a long-distance migratory songbird, the American redstart Setophaga ruticilla

Many species of birds exhibit brilliant ornamental plumage, yet most research on the function and evolution of plumage has been confined to the breeding season. In the American redstart Setophaga ruticilla , a long-distance Neotropical-Nearctic migratory bird, the acquisition of a winter territory in high-quality habitat advances spring departure and subsequent arrival on breeding areas, and increases reproductive success and annual survival. Here, we show that males holding winter territories in high-quality, black mangrove habitats in Jamaica have brighter yellow-orange tail feathers than males occupying territories in poor-quality second-growth scrub habitats. Moreover, males arriving on the breeding grounds from higher-quality winter habitats (inferred by stable-carbon isotopes) also had brighter tail feathers. Because behavioral dominance plays an important role in the acquisition of winter territories, plumage brightness may also be related to fighting ability and the acquisition and maintenance of territories in high-quality habitat. These results highlight the need for further research on the relationships between plumage coloration, behavior, and the ecology of over-wintering migratory birds.     

Sex-differentiated migration patterns, protandry and phenology in North European songbird populations

This study aims to investigate causes and mechanisms controlling protandrous migration patterns (the earlier breeding area arrival of males relative to females) and inter-sexual differences in timing of migration in relation to the recent climate-driven changes in phenology. Using standardised ringing data from a single site for eight North European migratory passerines collected throughout 22 years, we analysed sex-differentiated migration patterns, protandry and phenology of the entire populations. Our results show protandrous patterns for the first as well as later arriving individuals for all studied species. Males show more synchronous migration patterns compared to females and, hence, first arriving females followed males more closely than later arriving individuals. However, we found no inter-sexual differences in arrival trends as both sexes advance spring arrival over time with the largest change for the first arriving individuals. These findings seem in support of the “mate opportunity” hypothesis, as the arrival of males and females is strongly coupled and both sexes seem to compete for early arrival. Changes in timing of arrival in males and females as a response to climatic changes may influence subsequent mating decisions, with subsequent feedbacks on population dynamics such as reproductive success and individual fitness. However, during decades of consistent earlier spring arrival in all phases of migration we found no evidence of inter-sexual phenological differences.     

Antioxidants and condition-dependence of arrival date in a migratory passerine

Early arrival at the breeding area after spring migration determines several fitness benefits to migratory birds, including an early start of reproduction and a greater seasonal reproductive success. Environmental conditions determine the onset of migration at the population level, while physiological costs associated with migration and imposed on individuals determine the level of asynchrony in the pattern of arrival. These costs include several physiological changes, suppression of immune response, and an increased risk of oxidation by production of free radicals due to energetically expensive activities. According to the condition-dependent hypothesis of arrival date, only healthy individuals in prime condition can afford to arrive and thus reproduce early in the season.
We investigated condition-dependence of arrival date in male barn swallow ( Hirundo rustica L.), a migratory passerine, in two years that differed in environmental condition, and the role of carotenoids in mediating arrival date. We show that male tail length, the main secondary sexual character, body condition, and hematocrit were negatively correlated with arrival date in the first year, indicating better quality of early arriving males. In the second year, better environmental conditions advanced arrival of the entire population by weeks. In this season we could show no relationship between arrival and tail length or body condition. Moreover, a lower value of sedimentation rate and a brighter colour of the red throat feathers indicated better health status of the population. Arrival date is a condition-dependent character in barn swallows, since we found high repeatability of arrival date, lower values of carotenoids in blood and a lower depletion of carotenoids in blood shortly after arrival in early arriving males. This suggests that early arriving males either use fewer antioxidants for free radical scavenging, or they have differential access to antioxidants.     

Early arrival is not associated with more extra‐pair fertilizations in a long‐distance migratory bird

When assessing the benefits of early arrival date of migratory birds, a hidden and often ignored component of males’ fitness is the higher chance of early‐arriving birds to obtain extra‐pair fertilizations. Here we investigated how extra‐pair paternity might affect the relationship between male arrival date and number of fertilizations in a model study system, the European pied flycatcher Ficedula hypoleuca. For this purpose, we sampled and genotyped breeding pairs, unpaired males and offspring (including embryos from unhatched eggs when possible) of a Dutch pied flycatcher population. Detailed information on arrival date of males, egg laying date of their social mates and nest success was also recorded. Early‐arriving males had early‐laying females and males with early‐laying females had a higher probability of siring extra‐pair eggs and obtain more fertilizations. However, male arrival date alone did not correlate with the probability to gain extra‐pair paternity and neither to the amount of fertilized eggs. Both early‐ and late‐arriving males had a higher probability of losing paternity in their own nest compared to birds with an intermediate arrival date. Finally, late‐arriving males were more likely to remain unpaired but, interestingly, a few of these birds obtained paternity via extra‐pair copulations. Because earlier arrival date did not lead to more extra‐pair fertilizations and because such relationship seems to be driven mainly by the female's laying date, we conclude that the contribution of extra‐pair paternity to the overall fitness benefits of early male arrival date is relatively small.     

Protandrous arrival timing to breeding areas: a review

Protandry, the earlier arrival of males to breeding areas than females, is a common pattern of sex-biased timing in many animal taxa (e.g. some insects, fish, amphibians, reptiles, birds and mammals). The adaptive significance of protandry is not fully understood and, since the 1970s, at least seven hypotheses for protandry have been proposed. We describe each of these hypotheses and summarize what is known about each. In three of these hypotheses, the relative arrival timing of males and females has no direct fitness consequences for males or females, but selection for different timing in each sex indirectly produces protandry. In the other four hypotheses, the difference between male and female timing has fitness consequences for males or females and selection directly maintains the fitness-maximizing degree of sex-biased timing. The hypotheses are not mutually exclusive, and the degree of multiple mating by males and the occurrence of male territoriality seem to determine the relative importance of each hypothesis. In order to understand the adaptive significance of sex-biased timing, future studies need to consider all the alternatives and to assess the costs and benefits to males of early arrival relative to calendar date, to other males and to females.     

Arrival fat and reproductive performance in a long-distance passerine migrant

Long-distance passerine migrants deposit substantial fat stores to fuel their migratory journey. Many of those migratory birds arrive at their northerly breeding grounds with larger fat stores than were necessary to reach their breeding area. Both male and female American Redstarts ( Setophaga ruticilla) arrived to breed in Michigan's Upper Peninsula with fat, and females arrived with more fat than males in 2 out of 3 years. We test the hypothesis that migrants arriving at the breeding grounds with more body fat have higher reproductive success than birds arriving with little or no fat. Females, and to a lesser extent males, that arrive with fat experience gains in reproductive performance as evidenced by increased clutch size, egg volume, and nestling mass. The results have implications for understanding how events occurring during one phase of the annual cycle influence survival and/or reproductive performance in subsequent phases.     

Early arriving males wait longer for a mate than later arrivals: the case of a migratory monogamous passerine bird species

Individuals that arrive earlier on the breeding grounds may obtain many advantages but they also have to spend time waiting for a mate. I studied the waiting times of male red-breasted flycatchers Ficedula parva, a small, migratory, sexually dichromatic passerine bird species under natural conditions (Bia?owie?a National Park, Poland) in relation to year, arrival time, age of male and morphological parameters. The length of waiting time was dependent on males’ arrival time. The males which arrived later waited a shorter time for females than earlier arrivals. In some years older males spent more time waiting for mates than younger males, but in other years they waited for shorter times. A significant interaction between age of male and year was also observed. Despite the significantly earlier arrival of older males, the waiting time was not related to male age. The waiting time was also not related to body biometric parameters of the male. Despite waiting longer, early male red-breasted flycatchers have an advantage over later arrivals given this greater chance of mating.     

Temporal patterns of arrival from migration as a response to competition for breeding space

Birds arriving from spring migration have higher chances of securing a territory if they reach the breeding area before their companions. However, an early arrival may compromise their chances of surviving until reproduction begins. Here, we study how evolutionarily stable responses to these opposite constraints may shape patterns of arrival in a population of migratory birds, with the help of a simple evolutionary algorithm. We show that, initially, an increasing level of competition for breeding territories generates a massive peak of early arrivals. However, when the level of competition becomes very high, the temporal distribution of arrivals may take different shapes, depending on the modalities of competition. If individuals trying to usurp territories have relatively high chances of success, a second peak of arrival emerges at the very end of the arrival period. Birds arrive then in two successive waves. By contrast, if these chances are low, a single early peak of arrival is still present. Many individuals do however continuously arrive afterwards, at a regular and increasing tempo, until reproduction begins. The prior residence effect, that rules competition between resident birds and their challengers, is thus expected to influence the whole distribution of arrival dates on breeding grounds. This distribution will, in turn, affect the ability of the population to respond to changing environmental conditions.