Behavioral Ecology Advance Access originally published online on April 13, 2005
Behavioral Ecology 2005 16(4):755-762; doi:10.1093/beheco/ari049
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Reproductive asynchrony and population divergence between two tropical bird populations
a Department of Biology, 2119 Derring Hall, Virginia Tech, Blacksburg, VA 24061, USA, and b Department of Biology, University of Washington, Seattle, WA 98195, USA
Address correspondence to I. T. Moore. E-mail: itmoore{at}vt.edu.
Received 29 July 2004; accepted 15 March 2005.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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High-latitude vertebrates generally breed seasonally and synchronously as the primary environmental cue used to time seasonal processes is photoperiod. Investigations of tropical vertebrates have also documented seasonal reproduction, but it is unclear how synchronous reproduction is, both within and between populations. In this study, we investigated whether seasonal reproduction in a tropical species is synchronous between two populations in close proximity and, if not, whether asynchrony is correlated with genetic and cultural differentiation. We describe two equatorial populations of rufous-collared sparrows (Zonotrichia capensis), at the same latitude and separated by 25 km, that each breed seasonally but out of phase with each other. This asynchronous reproductive phenology is associated with local weather patterns and is independent of photoperiod. At a finer scale, reproductive timing is more highly synchronized within monogamous pairs than within the population as a whole. Associated with the difference in reproductive phenologies, we document that males in each population sing different song dialects. Using microsatellite DNA analysis, we found limited gene flow and significant genetic differentiation between the two populations. From these results we hypothesize that cultural and genetic differentiation between populations, which can be greater in tropical populations than temperate ones, can be associated with locally adapted reproductive phenologies.
Key words: biodiversity, bird, dialects, DNA, estrogen, evolution, microsatellite, migration rate, reproduction, song, speciation, testosterone, tropics, Zonotrichia capensis.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Seasonal reproduction synchronizes breeding with food abundance to maximize reproductive success (Lack, 1968
). Day length (hereafter referred to as photoperiod) has long been known to be crucial to the timing of seasonal processes (Gwinner, 2003). Photoperiodicity has been especially well studied in temperate-zone birds (Dawson et al., 2001) where the ultimately predictable change in the length of the day is the initial predictive cue used to time reproduction (Wingfield and Farner, 1993; Wingfield and Kenagy, 1991). Supplementary cues, such as food availability, temperature, and rainfall, are then used to fine-tune the timing of breeding to the local environment (Wingfield and Kenagy, 1991). The use of photoperiodic cues by animals increases with latitude and results in synchronized breeding, both within and among populations at the same latitude (Wingfield et al., 1997).
Mechanisms of seasonal reproduction in tropical species, including birds, have not been nearly as well studied as in temperate-zone species. Observational studies, in both the old and new world tropics, have described seasonal activities such as reproduction and molt but often without investigating the environmental cues used for timing and regional variation in timing (reviewed in Stutchbury and Morton, 2001). In addition, some tropical birds exhibit a circannual endogenous rhythm when kept in constant conditions (Gwinner and Dittami, 1990; Lofts, 1964) while others are sensitive to small changes (as little as 17 min) in photoperiod (Hau et al., 1998). Generally, breeding seasons tend to be longer in the tropics than in the temperate zone (Stutchbury and Morton, 2001). Correspondingly, the level of reproductive synchrony, both within and among populations, is expected to be lower in tropical populations due to the lack of environmental cues as predictable as photoperiod (Stutchbury and Morton, 2001). Because seasonally breeding equatorial populations may not have the opportunity to rely on changes in photoperiod to time reproduction, they must rely on other cues, such as food availability, rainfall, and/or temperature change. These cues vary locally, but can be predictable and reliable (e.g., Bendix and Rafiqpoor, 2001). This could lead to locally adapted breeding phenologies that vary on a much finer geographic scale than is observed at higher latitudes. Indeed, it is likely that many species and populations use a variety of environmental cues when determining when to breed.
It has recently been documented that, within species, populations at lower latitudes are more genetically divergent than those at higher latitudes (Martin and McKay, 2004). This is thought to be a proximate explanation (Martin and McKay, 2004) that results in the tropics being more biodiverse than the temperate zone (Willig et al., 2003). However, it is not well understood what factors contribute to the greater genetic divergence among populations initially. If reliance on environmental cues, other than photoperiod, for timing reproduction can promote reproductive asynchrony among populations, then locally adapted seasonal reproduction could be playing a crucial role in population differentiation. We predicted that in tropical populations, particularly near the equator, climatically distinct sites would promote breeding asynchrony among the resident populations. We also predicted that asynchronous reproduction among populations would then be associated with genetic and cultural isolation and divergence. To test these predictions, we investigated two equatorial populations of rufous-collared (also called chingolo or Andean) sparrows (Zonotrichia capensis) that are 25 km apart and experience different climatic conditions (Figure 1) but the same photoperiodic cues. We measured reproductive activity during four distinct times of the year and used microsatellite DNA analysis and recorded local song dialects to determine if the populations had diverged both genetically and culturally, respectively.
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Male Z. capensis in these two populations only sing during the breeding season (Moore et al., 2004c
), and males in each population sing a distinct dialect (Figure 2). The neural song-control system is plastic and is fully grown during the breeding season and regressed during the nonbreeding season (Moore et al., 2004c). The songs of Z. capensis are initiated with a series of note complexes (labeled as the theme in Figure 2) and terminated by a trill (labeled as the trill in Figure 2). Males in each population sing two song types, and individuals may switch song types during bouts of singing. Within both populations, the major difference between the two songs types is in the theme portion, with little difference in the trill. The theme portion may consist of two to three notes (Papallacta) or one to two notes (Pintag). All males in each population sing the local dialect with no apparent crossover between the populations. It is not known if males or females are able to discriminate between the song dialects.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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To investigate the relationships between reproductive phenology and population differentiation, we identified two populations of Z. capensis that are very close to the equator. These two sites are located near the towns of Papallacta and Pintag, Ecuador, and are hereafter referred to as such (Papallacta: 0° 21.7' S, 78° 9.0' W, 3300 m elevation; Pintag: 0° 22.6' S, 78° 22.5' W, 2900 m elevation). The two sites are approximately 25 km apart but are geographically separated by the Andean Divide (
4000 m). Being on the eastern (Papallacta) slope of the Andes and in an inter-Andean valley (Pintag), these two sites experience very different rainfall patterns (Figure 1, Bendix and Rafiqpoor, 2001). We initiated studies of Z. capensis in Papallacta in 2000 and later chose to study the population in Pintag based on published (Bendix and Rafiqpoor, 2001) climatic differences between the sites.
Breeding synchrony within equatorial populations
To investigate the level of breeding synchrony within the population, we determined the reproductive state of individuals in the Papallacta populations from 18 August to 12 September 2000. This is the prebreeding period during which individuals are recrudescing their gonads in anticipation of the upcoming breeding season. Individuals were captured and their reproductive state (testis length and width in males and diameter of the largest ovarian follicle in females) was determined by laparotomy and then released with an individual color band. Testis volume in males was calculated using a formula for ellipsoid cylinders (4/3
a2b where a is half the testis width and b half the length). We followed birds through observation and were able to identify seven pairs by observing close association between individuals. Identified pairs used for the analysis consisted of pairs that had been captured at close to the same time (mean = 1 day; range 0–4 days). We statistically compared the relationship between date and male testis volume to determine the level of breeding synchrony within the population and the relationship between male testis volume and the diameter of the female's largest ovarian follicle to determine the degree of breeding synchrony within pairs.
Reproductive seasonality and synchrony between equatorial populations
To investigate breeding seasonality between the populations, we documented the reproductive states of individuals in the Papallacta and Pintag populations during four different times during the year (February, April/May, August/September, October; see Table 1 for exact dates). During each of these trips, we went to one site first and subsequently visited the other site. Thus, the sites were investigated as closely as reasonably possible to the same time. During each period we passively caught individuals from each population in mist nets, primarily during the early morning. On capture, a 250-µl sample of whole blood was obtained from the alar wing vein of each individual. We also obtained measurements of body fat, wing length, body weight, cloacal protuberance length (an androgen-sensitive copulatory organ in males), and brood patch development (females). Body fat and brood patch were scored on a scale from 1 to 5 (for details of measurements see Wingfield and Farner, 1976). Blood samples were stored on ice until the end of each day when the plasma and red blood cells were separated through centrifugation and each frozen (plasma for hormone analyses and red blood cells for genetic analyses). We also compared the proportion of each population that was comprised of juveniles (juveniles have distinct plumage) during these four periods of the year using a log-linear analysis for a 3 x 3 contingency table.
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Blood samples were analyzed in duplicate by radioimmunoassay for testosterone in males and estradiol and progesterone in females (Moore et al., 2002
). Briefly, steroids were extracted from plasma using distilled dichloromethane and subsequently purified and separated by chromatography using diatomaceous earth columns. Plasma hormone concentrations were corrected for individual extraction efficiency. The average amount of plasma used in the assays was 107 µl (range 28–200 µl). The limits of detection for the assays averaged 0.05 ng/ml for testosterone, 0.23 ng/ml for estradiol, and 0.4 ng/ml for progesterone and depended on the volume of the plasma sample. The samples were run in four assays. Average intraassay variations were testosterone 13%, estradiol 9%, and progesterone 9%. Interassay variations were testosterone 14%, estradiol 14%, and progesterone 31%.
Statistical analyses on reproductive timing between the two populations were conducted separately on males and females. In both cases, a MANOVA was conducted with month (February, April/May, August/September, October), population (Papallacta, Pintag), and the interaction between the two as explanatory variables. The response variables were testosterone levels and cloacal protuberance length in males and estradiol levels, progesterone levels, and brood patch score in females. After the MANOVA, individual ANOVAs were conducted to determine where differences occurred. Statistically significant differences in the ANOVAs were based on sequential Bonferroni adjustments using the Dunn-
idák method (Sokal and Rohlf, 1995).
Genetic divergence
Twenty-four individuals (12 male, 12 female) from each population were genotyped at four neutral microsatellite loci. We extracted DNA from red blood cells using the Qiagen DNeasy Tissue Kit, following the manufacturer's instructions for extraction from nucleated blood cells. Primer sequences and annealing temperatures are summarized in Table 2. We amplified fragments at the four loci (Table 2) using 20-µl polymerase chain reactions (PCRs) containing 50 mM KCl, 10 mM Tris-HCl, 2.5 mM MgCl, 0.2 mM deoxynucleoside triphosphate, 0.5 µM of each primer, 0.5 units of polymerase, and 50 ng of template. The following thermal conditions were used for all loci: 94°C for 3 min followed by 33 cycles of 94°C for 40 s, annealing temperature (Table 2) for 40 s, 72°C for 40 s, and a final extension step of 72°C for 5 min. PCR products were separated on an Applied Biosystems 3100 capillary electrophoresis system.
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We performed tests of linkage disequilibrium and population differentiation and estimated FST and the number of migrants per generation using GENEPOP (Raymond and Rousset, 1995
). The Slatkin private allele method is the default method for estimating the number of migrants using GENEPOP (Slatkin, 1985). Recent levels of gene flow between the two sites were estimated using BayesAss (Wilson and Rannala, 2003) with 3.0 x 107 iterations and default values for burn-in and sampling frequency. We varied random seed numbers and prior distributions to test the robustness of our results. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Breeding synchrony within equatorial populations
During the prebreeding period there was individual variation in the timing of reproductive development, within the Papallacta population, independent of date (relationship between male testis volume and date: N = 81, R2 = .005, p = .52). However, within monogamous pairs there was a significant relationship between a male's testis volume and the diameter of the female's largest ovarian follicle (Figure 3, N = 7, R2 = .75, p = .012).
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Reproductive seasonality and synchrony between equatorial populations
For adult males, the MANOVA on reproductive factors demonstrated a significant effect of month, month by population, but not population alone (for statistics on all male reproductive factors, see Table 3 and Figure 4). For the subsequent ANOVAs, cloacal protuberance length varied significantly by month and month by population. Plasma testosterone levels in males exhibited a significant interaction between month and population. For adult females, the MANOVA on reproductive factors demonstrated a significant effect of month, population, and the interaction between the two (for statistics on all female reproductive factors, see Table 4 and Figure 5). For the subsequent ANOVAs, brood patch score varied significantly by month and month by population. Plasma progesterone and estradiol levels varied significantly by month.
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The proportion of each population that comprised juveniles changed between the sampling periods (Table 5). A log-linear analysis of a 3 x 3 contingency table (A = population [Papallacta, Pintag], B = month [February, April/May, August/September, October], C = age [adult, juvenile]) showed a significant interaction between the three terms (G2 = 81.58, df = 10, p < .0001). Population and month are dependent at each level of age (G2 = 45.44, df = 6, p < .0001). Population and age are dependent at each month (G2 = 18.14, df = 4, p = .0012). Finally, month and age are dependent at each population (G2 = 47, df = 6, p < .0001).
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Genetic divergence
We found that all four loci were unlinked. The two subpopulations were significantly genetically differentiated (G-based Fisher's combined probability test of differentiation,
2 = 32.61, df = 8, p = .00007). The estimate of FST was 0.014 and the number of migrants per generation was 2.33. The rates of gene flow between the two populations are summarized in Table 6. The posterior distributions of migration rate were not sensitive to changes in random seed number or prior distribution estimates.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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This study suggests that reliance on cues other than photoperiod to time seasonal processes can result in locally adapted reproductive phenologies. Thus, population level reproductive phenologies can be asynchronous even between populations in close proximity if the environmental and climatic conditions vary. This asynchronous reproduction can also be associated with genetic and cultural isolation and divergence, although the causal factor is unknown. Allochronic speciation (speciation associated with different phenologies) has been previously described, especially in insects (e.g., Alexander and Bigelow, 1960
; Cooley et al., 2001, 2003), but to our knowledge it has not been described in birds. In the current system, it is not known if each population's reproductive phenology is genetically based or is a phenotypically plastic response to the local environment. If reproductive phenologies are genetically based (e.g., Gwinner and Dittami, 1990; Lambrechts et al., 1999), this could serve as an obvious barrier to gene flow between populations, promoting genetic differentiation. This potential reproductive isolating mechanism could then be a critical initial factor for future speciation. Locally adapted reproductive phenologies, even if a result of phenotypic plasticity, could result in genetic drift and divergence if the populations are not continuous. In this scenario, the barrier of the Andean Divide is likely responsible for both the asynchronous reproductive phenologies and genetic and cultural divergence. Often, reproductive phenology is governed by a combination of genetic and environmental factors (Gwinner, 2003; Lambrechts et al., 1999). Future studies will attempt to discern if the asynchronous reproduction between the sites is the result of genetically based endogenous rhythms or phenotypic plasticity. In either case, genetic or plastic, we hypothesize that locally adapted reproductive phenologies are a potential mechanism to help explain the greater genetic divergence among tropical populations, relative to temperate-zone populations, and the greater biodiversity in the tropics.
Breeding synchrony within equatorial populations
From our results, and those published previously (Moore et al., 2002, 2004a,b), it appears that breeding synchrony is greater within pairs than within populations. Both these equatorial populations of Z. capensis have extended breeding seasons, and not all individuals initiate seasonal gonadal growth at the same time. As such, there is a relatively large degree of within-population asynchrony at the beginning of the breeding season, in comparison with high-latitude species (Hahn et al., 1995; Hunt et al., 1995). This species is also socially monogamous (Miller and Miller, 1968). Thus, being able to synchronize reproductive stage within pairs facilitates successful reproduction. There is debate on the relationship between within-population breeding synchrony and the rates of extrapair fertilizations (EPF) (Schwagmeyer and Ketterson, 1999; Stutchbury and Morton, 2001). We do not currently know the EPF rate in these populations.
Social cues are used as supplementary factors to fine-tune the seasonal growth of gonads in temperate-zone species (Wingfield and Kenagy, 1991). Previous studies in closely related temperate-zone species have suggested that these social cues are hormonally mediated (Moore, 1982, 1983, 1984). It is probable that the breeding synchrony within pairs, that we describe, is mediated by social cues. It is unclear if these social cues are serving as supplementary cues or if one sex is simply driving the reproductive seasonality and the other is following. Future studies will investigate the hormonal and behavioral basis of reproductive synchrony within pairs.
Reproductive seasonality and synchrony between equatorial populations
Broad-level seasonal processes such as reproduction, territoriality, and molt have been previously described in tropical birds (for a review see Stutchbury and Morton, 2001). The current study documents seasonal reproduction in each of the two populations investigated. We conclude that the reproduction is truly seasonal and asynchronous in nature, and not opportunistic, because the same pattern has been observed over 4 years in Papallacta and over 2 years in Pintag. In addition, the gonads are fully regressed during nonbreeding periods, suggesting that the birds are truly unable to breed during those times of the year and every individual in the population is following the same general schedule. Molt also occurs asynchronously between the two populations (Moore, personal observation). The reproductive pattern we describe is also accompanied by changes in brain structure that are thought to be associated with seasonal reproduction. The size and structure of the neural song-control system in these birds changes seasonally and asynchronously between these populations (Moore et al., 2004c) as does the hypothalamic gonadotropin-releasing hormone system (Moore IT, Bonier F, Wingfield JC, in preparation).
The fact that the reproductive cycle is consistent year to year suggests that breeding is being driven by either an endogenous rhythm, some factor in the environment, or a combination of both (Gwinner, 2003). While it would be novel, the environmental factor could be serving as a circannual zeitgeber (an environmental factor used to entrain biological rhythms such as annual cycles) to set the clock (Scheuerlein and Gwinner, 2002). This has been previously discussed as a mechanism tropical birds could use to time seasonal processes in environments lacking the predictable photoperiodic cues (Gwinner, 2003). At this point, it is unclear whether the differences in timing of breeding between the populations are due to genetically based differences between the populations, phenotypic plasticity, or a combination of both.
Seasonal reproduction in these populations is most likely occurring independent of photoperiod, but it is unclear what the relevant environmental cues are. It is unknown if seasonal changes in timing of dawn and dusk are important for these birds (Borchert et al., 2005). While even small changes in photoperiod can mediate gonad growth in tropical birds (Hau et al., 1998), it is unlikely that the slight changes that occur at the two field sites, so close to the equator, are perceptible. In addition, the fact that the breeding schedules are asynchronous in the two populations, despite the fact that they are found at the same latitude, further suggests that the birds are relying on environmental cues other than photoperiod.
It is possible that the two populations (1) rely on the same cue, which is timed differently between the sites; (2) rely on different cues; or (3) rely on the same cue, which is timed the same, but stimulates different responses. Rainfall patterns are different between these two sites despite their close proximity (Figure 1). It is possible that seasonal changes in food supply rather than, but associated with, rainfall pattern are responsible for the timing of reproduction in these two populations. In another tropical species, the Seychelles warbler (Acrocephalus sechellensis), food supply appears be an important determinant of seasonal reproductive patterns (Komdeur, 1996). Birds transferred to islands with higher food availability extended their breeding seasons and produced more broods of young.
However, there does appear to be an endogenous basis for some seasonal reproduction in tropical birds (Gwinner, 2003). While food availability can modify the timing of reproduction, it does not appear to be the zeitgeber and seasonal processes continue in constant conditions (Gwinner and Dittami, 1990; Scheuerlein and Gwinner, 2002). Other studies in midlatitude species (blue tits, Parus caeruleus) have documented population differences in breeding phenology in populations at the same latitude (Lambrechts and Perret, 2000; Lambrechts et al., 1996). While there appears to be a genetic difference in response to photoperiod cues, the birds are also using food cues to modify the timing of reproduction (Lambrechts et al., 1999).
Population divergence
These two populations, separated by 25 km, have diverged both genetically (microsatellite DNA) as well as culturally (song dialects). It is worth noting that both these populations are point samples within much larger populations that exist on both slopes of the Andes but are not locally continuous due to the Andean Divide. Members of the genus Zonotrichia are typically good dispersers and have relatively low population levels of genetic structuring (Soha et al., 2004), although the populations we studied are nonmigratory. Our results for FST are similar to those published for other members of the genus despite the use of similar (Soha et al., 2004) and dissimilar techniques (Lougheed and Handford, 1992; Soha et al., 2004). As our samples were obtained at sites within two, probably very large and genetically diverse populations on either slope of the Andes, FST is not expected to be high (O'Reilly et al., 2004). The presence of multiple private alleles and limited migration rates (Table 6) suggest high levels of isolation for populations in such close proximity. It is also worth noting that documenting genetic divergence at neutral loci suggests that even greater divergence would be seen using quantitative genetic trait variation (Qst) as Qst is typically larger than FST (McKay and Latta, 2002). We would predict that genetic divergence would be lower among equidistant populations on each slope of the Andes than among populations across the slope.
We do not know the cause and effect relationships between reproductive asynchrony, cultural divergence, genetic divergence, and the geological barrier of the Andean Divide. It seems likely that the Andean Divide has caused both the reproductive asynchrony and the genetic divergence between the two populations. This could result from the divide altering weather patterns (Figure 1) and thus optimal periods for reproduction, or the divide could be serving as a high-elevation geological barrier to dispersal. The upper elevation limit for breeding Z. capensis in Ecuador is 3500 m (Ridgley and Greenfield, 2001) and the lowest local pass is 4000 m. It would be difficult to discriminate which function of the divide is most important for the genetic divergence between the populations. It is also possible that an unidentified factor is responsible for the genetic divergence between the populations.
While there is little previous information on breeding synchrony and genetic relatedness, there is more information on the relationship between culturally transmitted behaviors, such as song dialects, and genetic relatedness (Baptista and Trail, 1992). Vocal dialects and genetic differentiation have been extensively studied in birds of the genus Zonotrichia. Despite a number of studies, in a number of species and subspecies of Zonotrichia, investigators have found little effect of dialect on population genetic differentiation (Lougheed and Handford, 1992; Lougheed et al., 1993; Soha et al., 2004). The sole exception seems to be the mountain white-crowned sparrow (Zonotrichia leucophrys oriantha), where there was a small but significantly greater amount of genetic variation among dialect areas than among sites within a dialect (MacDougall-Shackleton EA and MacDougall-Shackleton SA, 2001). Dialect variation has been well documented in Z. capensis (Handford and Lougheed, 1991; Lougheed et al., 1989; Nottebohm, 1969, 1975). However, no relationship has been found between genetic variation and dialects in Z. capensis (Lougheed and Handford, 1992; Lougheed et al., 1989, 1993). Thus, it appears that the current results are an example of genetic divergence with song dialects, although it is likely that the asynchronous reproduction between the populations plays a role.
In summary, this study documents high levels of divergence in multiple factors between tropical bird populations in close proximity. Reproduction is seasonal in each population with high levels of synchrony within monogamous pairs. Between the two populations there is divergence in song dialects, reproductive phenology, and neutral genetic markers. It is, as yet, unknown what are the causal factors and what factors are the effects. However, the results do suggest that local adaptation can occur among populations in close proximity in the tropics, especially when photoperiodic cues are not used to organize seasonal processes, and this can be associated with genetic and cultural divergence. This divergence could help explain the greater genetic divergence among populations, and the greater biodiversity, in the tropics in comparison to the temperate zone.
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ACKNOWLEDGEMENTS |
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We would like to thank the following people for assistance in the field and laboratory: Lisa Belden, Shallin Busch, Darren Lerner, Nicole Perfito, Beth Ramage, Haruka Wada, and Brian Walker. We also thank Toby Bradshaw, Ray Huey, Holly Goyert, Paul Martin, Paige Warren, and Greg Wilson for useful comments on the genetic analyses and earlier versions of the manuscript. We would like to thank the Fundación Antisana, Fundación Terra, Termas de Papallacta, and Patricio Muñoz for field arrangements. We thank L. Erckmann for steroid assay assistance. This research was approved by the University of Washington IACUC and supported by NSF IBN-9905679 to J.C.W. and a Franklin Research Grant from the American Philosophical Society to I.T.M. I.T.M. was supported by a NSF Postdoctoral fellowship (DBI-9904144) and a Society for Neuroscience Postdoctoral fellowship (T32 MH20069).
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