Eugene S. Morton

The effect of breeding synchrony on extra-pair mating systems in songbirds

Extra-pair mating systems are now considered to be typical of songbirds because DNA fingerprinting has revealed high rates of extra-pair fertilizations (EPFs) in so many species previously thought to be monogamous. However, there is no general framework to explain the tremendous variability among songbirds in EPF rate. Here, in a comparison of EPF rates and temporal patterns of nesting among songbirds, we show that EPFs are most common in species where females breed synchronously. We argue that for both males and females, a temporal concentration of female fertility (breeding synchrony) increases the net benefits of seeking EPFs. One implication of this finding is that tropical songbirds, most of which breed asynchronously, are predicted to have low levels of extra-pair matings. Testes size is positively correlated with frequency of EPFs, and as predicted, tropical songbirds had small testes size relative to temperate zone species. The few DNA fingerprinting studies that exist for socially monogamous tropical songbirds support the correlation between breeding synchrony and EPFs. We believe that breeding synchrony is the most important factor promoting the evolution of extra-pair mating systems.

Extrapair fertilizations and the evolution of colonial breeding in purple martins

We used DNA fingerprinting to show that, in Purple Martins (Progne subis), forced extrapair copulations (FEPC) result in age-biased extrapair fertilizations. Older males achieved 96% paternity of their broods and increased their fecundity at the expense of young males, which achieved only 29% paternity. Older males recruit young males and females to unused nesting cavities that they had previously defended against other older males. Each year, nearly half (45%) of the breeding martins were recruited young birds not born in the colony. Recruitments are individually timed and begin when each older males mate has completed a nest. Adult males may have accrued an average of 3.6 fertilized eggs through forced extrapair copulations in addition to eggs produced by their mates (4.5 eggs) for an overall average of 8.1. Noncolonial males without the opportunity for FEPCs would suffer 44% lower lifetime fecundity. Thirty-six percent of the eggs in the nests of young males were the result of egg parasitism, the significance of which is unstudied. These findings support the hypothesis that colonial breeding evolved in Purple Martins to increase the opportunity for extrapair fertilizations. Martins may be an extreme example of a general trend in breeding systems where migration and temperate climate concentrate fertile females in time and space. Received 26 May 1989, accepted 12 October 1989.

Condition-dependent control of paternity by female purple martins: implications for coloniality

Abstract Proposed causal links between extra-pair copulation (EPC) and colony formation in socially monogamous birds hinge on the question of which sex controls fertilizations. We examined in colonial purple martins Progne subis (1) whether EPCs were forced or accepted by females, and (2) the degree to which apparently receptive females were able to obtain EPCs against their mates’ paternity defenses. Paternity analyses of multilocus DNA fingerprinting confirmed previous findings of a marked relationship between age class and extra-pair fertilizations (EPFs), with young males losing paternity of 43% (n = 53) of their putative offspring compared to 4% (n = 85) by old males. All assignable extra-pair offspring were sired by old males, with one male obtaining most EPFs each year. Contrary to the hypothesis that EPCs are forced, EPF frequency within age class did not increase with seasonal increases in the number of males per fertile female. Whereas the male control hypothesis predicted that the male age class that mate-guarded more would be cuckolded less, the reverse was true: young males guarded significantly more intensely. The male age class difference in cuckoldry could not be explained by the possibility that young and inexperienced females (which are usually paired to young males) were more vulnerable to forced copulation because EPFs were unrelated to female age. These findings suggest that females (1) pair with old males and avoid EPCs, or (2) pursue a mixed mating strategy of pairing with young males and accepting EPCs from old males. The receptivity to EPCs by females paired to young males put them in conflict with their mates. Two factors determined the paternity achieved by young males: (1) the relative size of the male to the female, with young males achieving much higher paternity when they were larger than their mates, and (2) the intensity of mate-guarding. Both variables together explained 77% of the variance in paternity and are each aspects of male-female conflict. Given female receptivity to EPCs, mate-guarding can be viewed as male interference with female mating strategies. We conclude that EPCs are rarely or never forced, but the opportunity for females paired to young males to obtain EPCs is relative to the ability of their mates to prevent them from encountering other males. Evidence of mixed mating strategies by females, combined with other features of the martin mating system, is consistent with the female-driven “hidden lek hypothesis” of colony formation which predicts that males are drawn to colonies when females seek extra-pair copulations.

On the learning of degraded and undegraded songs in the Carolina wren

Adult male Carolina wrens (Thyrothorus ludovicianus) are known to use degradation in the songs they hear to estimate their distance from a singing conspecific. They also sing songs that are structured to prevent degradation owing to acoustic features particular to specific habitats. Here we ask if acoustically isolated, naive young wrens use sound degradation as a cue in choosing songs to learn. All four isolated birds learned significantly more undegraded than degraded songs, showing that song degradation is perceived and used by naive birds. We suggest that the attention given to song degradation by young birds learning songs produces a proximate mechanism to explain the common occurrence of song sharing by territorial neighbours and supports the ranging hypothesis (Morton 1982). Sufficient evidence now exists to suggest that sound degradation, and the ability of birds to use it, should be taken into account in studies using responses to playback of bird song.

VOCAL RESPONSE TO PREDATORS IN PAIR-BONDED CAROLINA WRENS

The Carolina Wren (Thryothorus ludovicianus) has a social system that is much more characteristic of tropical than temperate zone species. Males and females form permanent pair bonds (Bent 1948, Thomas 1953, and pers. observ. of a color-banded population over 4 years) and pairs defend a territory throughout the year. Probably due to this social system, Carolina Wrens use all of their vocal signals throughout the year (Morton, in press). Here we present data derived from field observations and laboratory experiments on one of this wrens vocal signals, which we term the chirt. Carolina Wren chirts are structurally variable and are delivered in temporally variable ways. We hope to explain here how this call varies and how its variation is adaptive within the Carolina Wrens social system. Since chirt calls depart from the commonly held view that most bird sounds are rather discrete (Marler 1967, Smith 1968, 1969), a discussion of them may shed new light on sources of selection favoring graded communication systems.

RECENT ADVANCES IN THE BEHAVIORAL ECOLOGY OF TROPICAL BIRDS The 2005 Margaret Morse Nice Lecture

Abstract Tropical birds offer unique opportunities to test ecological and evolutionary theory because their life history traits are so diverse and different from temperate zone models upon which most empirical studies are based. We review recent studies on the behavioral ecology of tropical birds, studies that explore new advances in this field. Life histories and their evolution remain the focus of research on tropical birds. Clutch size manipulations in two species showed that food limitation does not explain small clutch size. In antbirds, enlarged clutches decreased post-fledging survival whereas in thrushes, enlarged broods were costly due to high nest predation. Small clutches may be favored via different ultimate selective forces and shared underlying tradeoffs between the immune, metabolic, and endocrine systems in the body may account for the commonly observed ‘slow pace of life’ in tropical birds. The physiological tradeoff between testosterone and immunocompetence may explain the evolution of low testosterone levels in tropical passerines where adult survival is paramount. In contrast to life history theory, few studies have explored temperate-tropical differences in territoriality, mating systems, and song function. The idea that low breeding synchrony in tropical birds is associated with low levels of extra-pair fertilizations was supported by several new paternity studies conducted on tropical passerines. Seasonally breeding tropical birds have higher testosterone levels than tropical birds with prolonged breeding seasons, although it is unclear if this pattern is driven by mating systems per se or selection from pathogens. Recent work on relations between pair members in permanently paired tropical passerines focuses on the question of mate defense versus territorial defense and the extent of cooperation versus selfish interests in inter-sexual relations.

Song ranging by the dusky antbird, Cercomacra tyrannina : ranging without song learning

Abstract In a population of dusky antbirds (Cercomacra tyrannina), less aggressive responses to distance-degraded playbacks than to undegraded playbacks of pair duets show that this tropical suboscine passerine uses sound degradation to range distance from singing conspecifics. This is the first example of song-ranging in a species that does not learn songs, supporting the hypothesis that ranging preceded the song learning that occurs in more recently evolved passerine birds (oscines). Both sexes sing and are able to use song degradation to range distance from singers when their sex-specific song is played back.

Extra-pair mating system of a synchronously breeding tropical songbird

Extra-pair matings are now recognized as a fundamental component of avian mating systems. However, in tropical regions where breeding is typically asynchronous socially monogamous species appear to have low sperm competition and few extrapair matings. We predicted that if breeding synchrony promotes the evolution of extra-pair matings, then tropical species that breed synchronously, like the Claycolored Robin Turdus grayi, should have abundant extra-pair young (EPY). Breeding began relatively abruptly during the dry season (Feb-Mar) in this non-migratory species, with a mean of 25% of females fertile on a given day. Overall, 53% of females produced EPY, and 38% of nestlings were EPY. Males have a long and conspicuous dawn chorus, which could be a result of intense male-male competition for extra-pair matings. Male songs are individually recognizable and males vary greatly in song output. Male song output declined significantly from the pre-nesting stage through the incubation stage, as would be expected if song is important in mate choice. Our results support the idea that breeding synchrony favors extra-pair matings, however further studies of tropical songbirds are needed to fully explore how ecology is tied to extra-pair mating systems.

Variation in mate guarding intensity by male purple martins

The frequency with which individual male purple martins (Hirundinidae: Progne subis) guard their mates during forays to gather nest material varies from 0 to 100%. During such forays, guarding males accompany their mates continuously from the time a female leaves the nest site until she returns to the nest site with nest material. Non-guarding males do not accompany females on these collecting forays. Unguarded females are subject to forced extrapair copulation attempts on almost all of their forays to collect nest material. Because this suggested that non-guarding males may have a lowered assurance of paternity relative to guarding males, I asked if mate guarding frequency is directly related to parental care. However, male parental effort, as assessed by feeding rates, was not related to mate guarding intensity. Mate guarding intensity may vary widely among individual male martins since nest site defense may preclude guarding in some and superiority in sperm competition by means other than exclusive access to females may reduce their chances of being cuckolded.

No Evidence for Acoustic Mate-Guarding in Duetting Buff-Breasted Wrens (Thryothorus Leucotis)

There are few empirical tests of the acoustic mate-guarding hypothesis for the function of duetting in birds. This hypothesis states that when females are fertile, males initiate many songs or answer most of their mates’ solo songs to form duets and repel rival males seeking extra-pair copulations. We tested the hypothesis by comparing song initiation and answer rates of males and females in socially monogamous buff-breasted wrens (Throthorus leucotis) during pre-fertile and fertile periods. During pre-fertile periods, males often sang for short periods before being answered by their mates, yet first duets were formed earlier relative to dawn and more duets were given during the dawn chorus on pre-fertile than fertile mornings. Males initiated more songs during pre-fertile than fertile periods, whereas there was no difference between stages in female song initiation rates. The proportion of songs answered by individuals of both sexes did not differ between breeding stages. Other mate-guarding behaviours, such as frequent copulation and maintaining close proximity to mates when fertile, did not appear to be important in this species, as no copulations were observed and there was no difference in the time pairs spent in close proximity when females were fertile or not. Parentage analysis revealed that only 3% of 31 broods had young that were likely the result of extra-pair paternity. These findings do not support the acoustic mate-guarding hypothesis, and suggest that the low rate of extra-pair paternity in buff-breasted wrens was maintained without the use of acoustic or traditional paternity guards.