Randomization Analyses: Mimicry, Geographic Variation and Cultural Evolution of Song in Brood-Parasitic Straw-Tailed Whydahs, Vidua fischeri

Although bird song has been an important model for investigating questions of behavior development, cultural evolution and population differentiation, the quantitative methods of analysis have been problematic. Here we develop and apply quantitative randomization methods to test hypotheses about these processes in a natural population of birds. Songs of the African brood-parasitic straw-tailed whydahs ( Vidua fischeri ) and songs of their host species, the purple grenadier ( Granatina ianthinogaster ), were compared in audiospectrograms for similarity to test the following hypotheses: Whydahs mimic the songs of their host species, they have local song dialects, neighboring males match their song themes, local males match the songs of local hosts, remote populations have different songs according to their geographic distance, and songs undergo cultural evolution over time across generations. Randomization analyses were completed using (1) Mantel matrix statistics and (2) tree-based measures employing Sankoff optimization of Manhattan matrices and approximate randomizations. Our results provide evidence for song mimicry, local song dialects, matching song themes between neighboring males, song matching of local whydah mimics and grenadier song models, correspondence of song differences and geographic distance, and cultural continuity with change in song traditions within a local population. These randomization methods may be useful in other studies of animal communication, and they are sufficiently general for use both with distance matrices derived either from naturalistic impressions of song similarity as in our example or from acoustic measurements.     

Vocal dialects, sex-biased dispersal, and microsatellite population structure in the parrot Amazona auropalliata

Geographic variation in microsatellite allele frequencies was assessed at nine sites in two regional vocal dialects of the parrot Amazona auropalliata (yellow-naped amazon) to test for correspondence between dialects and population structure. There was no relationship between the genetic distances between individuals and their dialect membership. High rates of gene flow were estimated between vocal dialects based on genetic differentiation. In addition, 5.5% of pairs of individuals compared across the dialect boundary were estimated to be related at the level of half siblings, indicating that dispersal is ongoing. The number of effective migrants per generation between dialects estimated with the microsatellite data was roughly one-seventh the number estimated with mitochondrial control region sequence data from the same individuals, suggesting that gene flow may be female-biased. Together, these results suggest that the observed mosaic pattern of geographic variation in vocalizations is maintained by learning of local call types by immigrant birds after dispersal. We found no evidence that ongoing habitat fragmentation has contributed to cryptic population structure.     

Cultural and genetic evolution in mountain white-crowned sparrows: song dialects are associated with population structure

Bird song often varies geographically within a species; when this geographic variation has distinct boundaries, the shared song types are referred to as song dialects. How dialects are produced and their adaptive significance are longstanding problems in biology, with implications for the role of culture in the evolution and ecology of diverse organisms, including humans. Here we test the hypothesis that song dialect, a culturally transmitted trait, is related to the population genetic structure of mountain white-crowned sparrows (Zonotrichia leucophrys oriantha). To address this, we compared microsatellite allele frequencies from 18 sample sites representing eight dialect regions in the Sierra Nevada. Pairwise genetic distances were not significantly correlated with geographic distances either within or between dialects, nor did dialect groups form distinct genetic groups according to neighbor-joining or UPGMA analysis, and most variation in allele frequencies occurred among individuals rather than at higher levels. However, most of the remaining variation was attributable to differences among, rather than within, dialect regions, and this among-dialect component of variance was statistically significant. Moreover, when controlling for the effect of geographic distance, song dissimilarity and genetic distance between site pairs were significantly correlated. Thus, song dialects appear to be associated with reductions in, but not strict barriers to, gene flow among dialect regions.     

Multiple regression on distance matrices: a multivariate spatial analysis tool

I explore the use of multiple regression on distance matrices (MRM), an extension of partial Mantel analysis, in spatial analysis of ecological data. MRM involves a multiple regression of a response matrix on any number of explanatory matrices, where each matrix contains distances or similarities (in terms of ecological, spatial, or other attributes) between all pair-wise combinations of n objects (sample units); tests of statistical significance are performed by permutation. The method is flexible in terms of the types of data that may be analyzed (counts, presence–absence, continuous, categorical) and the shapes of response curves. MRM offers several advantages over traditional partial Mantel analysis: (1) separating environmental distances into distinct distance matrices allows inferences to be made at the level of individual variables; (2) nonparametric or nonlinear multiple regression methods may be employed; and (3) spatial autocorrelation may be quantified and tested at different spatial scales using a series of lag matrices, each representing a geographic distance class. The MRM lag matrices model may be parameterized to yield very similar inferences regarding spatial autocorrelation as the Mantel correlogram. Unlike the correlogram, however, the lag matrices model may also include environmental distance matrices, so that spatial patterns in species abundance distances (community similarity) may be quantified while controlling for the environmental similarity between sites. Examples of spatial analyses with MRM are presented.     

Geographic song discrimination in relation to dispersal distances in song sparrows

Whether geographic variation in signals actually affects communication between individuals depends on whether discriminable differences in signals occur over distances that individuals move in their lifetimes. We measure the ability of song sparrows (Melospiza melodia) to discriminate foreign from local songs using foreign songs recorded at a series of increasing distances and compare the results with previous measurements of dispersal distances. We test discrimination in males using playback of songs on territories and measuring approach and in females using playback to estradiol-treated captives and measuring courtship display. Females fail to discriminate against foreign songs recorded at 18 km but do discriminate against foreign songs recorded at 34, 68, 135, and 540 km. Males fail to discriminate against foreign songs recorded at 18, 34, 68, 135, and 270 km but do discriminate against foreign songs from 540 km. Females are more discriminating, but even they do not discriminate at a distance three times the root-mean-square dispersal distance, as estimated from mtDNA variation. We suggest that female preference for local songs benefits females not because it allows them to reject foreign males but because accurate production of local song serves as a test of song-learning ability.     

The interplay of within-species perceptual predispositions and experience during song ontogeny in zebra finches (Taeniopygia guttata)

Vocal acquisition in songbirds and humans shows many similarities, one of which is that both involve a combination of experience and perceptual predispositions. Among languages some speech sounds are shared, while others are not. This could reflect a predisposition in young infants for learning some speech sounds over others, which combines with exposure-based learning. Similarly, in songbirds, some sounds are common across populations, while others are more specific to populations or individuals. We examine whether this is also due to perceptual preferences for certain within-species element types in naive juvenile male birds, and how such preferences interact with exposure to guide subsequent song learning. We show that young zebra finches lacking previous song exposure perceptually prefer songs with more common zebra finch song element types over songs with less common elements. Next, we demonstrate that after subsequent tutoring, birds prefer tutor songs regardless of whether these contain more common or less common elements. In adulthood, birds tutored with more common elements showed a higher song similarity to their tutor song, indicating that the early bias influenced song learning. Our findings help to understand the maintenance of similarities and the presence of differences among birds'' songs, their dialects and human languages.     

Limited genetic differentiation between acoustically divergent populations of urban and rural silvereyes (Zosterops lateralis)

The bioacoustic attributes of vocalisations made by birds in urban environments often differ markedly from those of rural conspecifics. Whether such differences are result from genetic divergence between urban and rural populations, or from plasticity or cultural evolution of song remains poorly understood. Silvereyes (Zosterops lateralis) show evidence of acoustic adaptation to urban noise, modifying both their songs and calls in cities when compared to rural areas. We investigated whether these differences were associated with corresponding morphological and neutral genetic differences. Across six pairs of geographically separate urban and rural populations, all morphological traits measured were similar. Furthermore, genetic analyses of variation at nine microsatellite loci revealed high levels of genetic connectivity between populations, and similar levels of heterozygosity in both habitat types. Consistent directional shifts in song attributes of city birds across large geographic areas thus do not appear to be accompanied by associated morphological or neutral genetic divergence.     

Quantitative matrix comparisons in ecological and evolutionary investigations

The pair-wise statistical comparison of data matrices is a methodological problem which must be dealt with in a variety of disciplines. In this report we demonstrate an innovative approach using the Mantel test (a nonparametric, multivariate evaluation of test matrices) to quantitatively contrast observed color polymorphisms in male Poecilia reticulata collected from 41 samples sites in Trinidad against four evolutionary models: (1) response to an environmental gradient, (2) localized environmental patches, (3) isolation by distance, and (4) historical factors. To represent these models we derived pair-wise distances between study sites for the following data: (1) altitude, (2) density of predators, and (3) kilometric distances. To represent model four above, we generated an imposed asymptotic distance matrix for geographically contiguous sites, and a Gabriel connectivity matrix for stream-connected sites (e.g. those within the same watershed). We found that differences in color polymorphisms covary significantly with differences in predator densities and in altitudes, suggesting that male color polymorphisms track clinally distributed communities of visually hunting predators. These data substantiate previously published results from field and laboratory experiments. The utility of the Mantel procedure is that it permits a quantitative evaluation of ecological and evolutionary problems which have previously been difficult to approach statistically.     

Genetic population structure in an equatorial sparrow: roles for culture and geography

Female preference for local cultural traits has been proposed as a barrier to breeding among animal populations. As such, several studies have found correlations between male bird song dialects and population genetics over relatively large distances. To investigate whether female choice for local dialects could act as a barrier to breeding between nearby and contiguous populations, we tested whether variation in male song dialects explains genetic structure among eight populations of rufous‐collared sparrows (Zonotrichia capensis) in Ecuador. Our study sites lay along a transect, and adjacent study sites were separated by approximately 25 km, an order of magnitude less than previously examined for this and most other species. This transect crossed an Andean ridge and through the Quijos River Valley, both of which may be barriers to gene flow. Using a variance partitioning approach, we show that song dialect is important in explaining population genetics, independent of the geographic variables: distance, the river valley and the Andean Ridge. This result is consistent with the hypothesis that song acts as a barrier to breeding among populations in close proximity. In addition, songs of contiguous populations differed by the same degree or more than between two populations previously shown to exhibit female preference for local dialect, suggesting that birds from these populations would also breed preferentially with locals. As expected, all geographic variables (distance, the river valley and the Andean Ridge) also predicted population genetic structure. Our results have important implications for the understanding whether, and at what spatial scale, culture can affect population divergence.     

Multiple Mantel tests and isolation-by-distance, taking into account long-term historical divergence

Mantel tests of matrix correspondence have been widely used in population genetics to examine microevolutionary processes, such as isolation-by-distance (IBD). We used partial and multiple Mantel tests to simultaneously test long-term historical effects and current divergence and equilibrium processes, such as IBD. We used these procedures to calculate genetic divergence among Eugenia dysenterica (Myrtaceae) populations in Central Brazil. The Nei's genetic distances between pairs of local populations were strongly correlated with geographic distances, suggesting an IBD process, but field observations and the geographic distribution of the samples suggest that populations may have been subjected to more complex evolutionary processes of genetic divergence. Partial Mantel regression was used to partition the effects of geographic structure and long-term divergence associated with a possible historical barrier. The R(2) of the model with both effects was 73.3%, and after the partition 21.9% of the variation in the genetic distances could be attributed to long-term historical divergence alone, whereas only 1.5% of the variation in genetic distances could be attributed to IBD. As expected, there was a large overlap between these processes when explaining genetic divergence, so it was not possible to entirely partition divergence between historical and contemporary processes.     

Winter dialects in the bronzed cowbird and their relationship to breeding-season dialects

Studies of geographical variation in animal signals generally focus on breeding-season behaviour but, in many species, signalling persists throughout the year. In passerine birds, patterns of variation in the nonbreeding season might provide opportunities for vocal learning that have been neglected by a historic focus on breeding-season behaviour. This study provides the first example of dialect variation outside of the breeding season. Quantitative analysis of acoustic similarity showed discrete differences between the songs of bronzed cowbirds, Molothrus aeneus, in four winter flocks. Most songs produced by members of a given flock were classified as belonging to the same dialect. Songs from one of the four winter dialects were indistinguishable from songs recorded in the breeding season in the same region. Depending on migratory patterns, dialects in one season may be a consequence of dialects in the other season, or the two seasonal patterns may be the result of independent social or evolutionary forces. Because the nonbreeding season is an important period of vocal learning in some bird species, winter dialects might limit the range of signals available for individuals to learn to produce. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

From song dialects to speciation in white‐crowned sparrows

The behavioural signals used in mate selection are a key component in the evolution of premating isolating barriers and, subsequently, the formation of new species. The importance of mating signals has a long tradition of study in songbirds, where many species differ in their song characteristics. In oscine songbirds, individual birds usually learn their songs from a tutor. Mistakes during learning can help generate geographic dialects, akin to those within human language groups. In songbirds, dialect differences can often be substantial and there is an intuitive connection between the evolution of song amongst populations at a small scale, and the more substantive song differences between bird species and presumably used in species recognition. However, studies investigating the concordance between putative genetic and behavioural boundaries have generated mixed results. In many cases, this is possibly a function of the poor resolving power of the genetic markers employed. In this issue of Molecular Ecology, Lipshutz et al. ( 2017 ) combine genomic markers with a robust behavioural assay to address the importance of song variation amongst white‐crowned sparrow (Zonotrichia leucophrys) subspecies.     

Ecotypes and genetic structure of Rhinanthus alectorolophus (Orobanchaceae) in southwestern Germany

European annual species of the genus Rhinanthus often exhibit seasonal ecotypic variation, a phenomenon also known from related genera of hemiparasitic Orobanchaceae. Populations with different flowering times exist, correlated with differences in a number of morphological characters. The present study evaluates the correlation of morphological characters and genetic differentiation of populations of Rhinanthus alectorolophus. Thirty-nine populations of three different subspecies from southwestern Germany were sampled. A total of 798 individuals were used for morphological analyses and 187 of these for AFLP analyses. Principal component analysis showed that morphological variation is mostly continuous. In a discriminant analysis based on morphological characters, only 89.7 % of all individuals were correctly assigned to their previously determined subspecies, indicating that subspecies identification is ambiguous for some populations. Using AFLP data and Bayesian assignment analysis, the sampled individuals could be grouped in three genetic clusters which do not correspond to the three subspecies. Instead, the clustering shows a clear geographic pattern and a Mantel test likewise revealed a significant correlation between genetic and geographic distances. Correlations of genetic distances with differences in morphological characters were weak and mostly insignificant. The results indicate that the subspecies of R. alectorolophus do not form discrete entities and that the character combinations distinguishing them are homoplastic.     

Geographic variation of flower traits in Narcissus papyraceus (Amaryllidaceae): do pollinators matter?

Aim The geographic clinal variation of traits in organisms can indicate the possible causes of phenotypic evolution. We studied the correlates of flower trait variation in populations of a style‐dimorphic plant, Narcissus papyraceus Ker‐Gawl., within a region of high biogeographical significance, the Strait of Gibraltar. This species shows a geographic gradient in the style‐morph ratio, suggested to be driven by pollinator shifts. We tested whether parallel geographic variation of perianth traits also exists, concomitant with vegetative trait variation or genetic similarity of plant populations. Location The Strait of Gibraltar region (SG hereafter, including both south‐western Iberian Peninsula and north‐western Morocco). Methods We used univariate and multivariate analyses of flower and vegetative traits in 23 populations. We applied Mantel tests and partial Mantel correlations on vegetative and flower traits and geographic locations of populations to test for spatial effects. We used Moran’s autocorrelation analyses to explore the spatial structure within the range, and performed the analyses with and without the Moroccan samples to test for the effects of the SG on spatial patterns. Amplified fragment length polymorphism data were used to estimate the genetic distance between populations and to ascertain its relationship with morphometric distance. Results There was high variation between and within populations in both flower and vegetative traits. Mantel correlations between geographic and morphometric distances were not significant, but the exclusion of Moroccan populations revealed some distance effect. Partial Mantel correlation did not detect a significant correlation between flower and vegetative morphometric distances after controlling for geographic distance. There were opposite trends in spatial autocorrelograms of flower and vegetative traits. The genetic distance between pairs of populations was directly correlated with geographic distance; however, flower morphometric and genetic distances were not significantly correlated. Main conclusions The SG had some influence on phenotypes, although the causes remain to be determined. The opposite trend of variation in flower and vegetative traits, and the lack of correlation between genetic distance and dissimilarity of flower phenotypes favour the hypothesis of pollinator‐mediated selection on flower morphology, although this may affect only particular traits and populations rather than overall phenotypes. Although stochastic population processes may have a small effect, other factors may account for the high flower variation within and between populations.     

Hidden patterns of phylogenetic non‐stationarity overwhelm comparative analyses of niche conservatism and divergence

Aim Despite the importance of the niche concept in ecological and evolutionary theory, there are still many discussions about its definition and operational evaluation, especially when dealing with niche divergence and conservatism in an explicit phylogenetic context. Here we evaluate patterns of niche evolution in 67 New World Carnivora species, measured using Hellinger distances based on MAXENT models of species distribution. We show how inferences on niche conservatism or divergence depend on the way phylogenetic patterns are analysed using matrix comparison techniques. Innovation Initially we used the simplest approach of Mantel tests to compare Hellinger distances ( N ) derived from MAXENT and phylogenetic distances ( P ) among species. Then we extended the Mantel test to generate a multivariate correlogram, in which phylogenetic patterns are analysed at multiple levels in the phylogeny and can reveal nonlinearity in the relationship between divergence and time. Finally, we proposed a new approach to generate ‘local’ (or ‘specific’) leverages of components for Mantel correlation, evaluating the non‐stationarity in the relationship between N and P for each species. This new approach was used to show if some lineages are more prone to niche shift or conservatism than others. Main conclusions Standard Mantel tests indicated a poor correspondence between N and P matrices, discarding the idea of niche conservatism for Carnivora, but the correlogram supports that closely related species tend to be more similar than expected by chance. Moreover, the variance among Hellinger distances between pairs of closely phylogenetically related species is much larger than for the entire clade. Phylogenetic non‐stationarity analysis shows that in some Carnivora families the niche tends to divergence (Mustelidae and Canidae), whereas in others it tends to conservatism (Procyonidae and Mustelidae) at short phylogenetic distances. Our analyses clearly show that misleading results may appear if niche divergence is analysed only by simple matrix correlations not taking into account complex patterns of phylogenetic nonlinearity and non‐stationarity.     

Song learning: the interface between behaviour and neuroethology

The high degree of developmental plasticity displayed by the songs of oscine birds makes them appropriate subjects for research on the etiology and neurobiology of vocal learning. Strong individual differences and learned local dialects are common. The readiness to acquire new songs appears to persist throughout life in some species and is restricted to relatively short sensitive periods in others. Learning can occur with remarkably few exposures to song. Mimicry of other species occurs but, given a choice, there is a tendency to favour conspecific songs. Evidence is presented for two kinds of vocal learning, one 'memory-based', the other 'action-based.' Subsong and 'plastic song' phases of motor development appear to be obligatory steps in the ontogeny of learned songs. A case is made that acquisition and production should be viewed as distinct phenomena with different physiological correlates. Research on behavioural development is closely associated with studies of the physiology of development. The two are mutually synergistic, and the synergism is well displayed in research on song learning in birds. This review of some of the characteristics of avian vocal learning as derived from behavioural studies, indicates lacunae in our knowledge about the ethology of song learning, and suggests how the comparative study of vocal development can pave the way for new insights into the underlying neurobiology.     

Cultural interaction and biological distance in postclassic period Mexico

Economic, political, and cultural relationships connected virtually every population throughout Mexico during Postclassic period (AD 900–1520). Much of what is known about population interaction in prehistoric Mexico is based on archaeological or ethnohistoric data. What is unclear, especially for the Postclassic period, is how these data correlate with biological population structure. We address this by assessing biological (phenotypic) distances among 28 samples based upon a comparison of dental morphology trait frequencies, which serve as a proxy for genetic variation, from 810 individuals. These distances were compared with models representing geographic and cultural relationships among the same groups. Results of Mantel and partial Mantel matrix correlation tests show that shared migration and trade are correlated with biological distances, but geographic distance is not. Trade and political interaction are also correlated with biological distance when combined in a single matrix. These results indicate that trade and political relationships affected population structure among Postclassic Mexican populations. We suggest that trade likely played a major role in shaping patterns of interaction between populations. This study also shows that the biological distance data support the migration histories described in ethnohistoric sources. Am J Phys Anthropol 157:121–133, 2015. © 2015 Wiley Periodicals, Inc.     

Contrasting genetic structures in sister species of North American scrub-jays

Threatened Florida scrub-jays (Aphelocoma coerulescens breed communally, are restricted to xeric sandy scrub habitat, generally disperse fewer than three territory diameters. Closely related Western scrub-jays (A. californica) do not breed communally, have a broader habitat range, disperse greater distances, and are not threatened. We compared the genetic structure of 445 individuals in 11 populations in Florida with 157 individuals in eight populations of Western scrub-jays. At ten microsatellite loci, Florida had 24 out of 47 total alleles, while Western scrub-jays had 44. The Florida populations were more differentiated (G_ST = 0.048) than were a set of five California populations (G_ST = 0.015). A randomization extension of a Mantel test showed a stronger correlation between geographic and Cavalli-Sforza genetic distances among Western than Florida populations. Neighbour-joining trees clustered Florida populations from the same sandy ridge systems, suggesting that habitat continuity is more important than geographic proximity in allowing gene flow and preventing differentiation. For Western populations, isolation by distance appears to be the major determinant of genetic structure. Our results suggest that contrasting genetic structures may arise between closely related species, as a result of differences in ecology and social system. Conserving extant genetic variation in Florida jays will require maintaining viable populations in each of the major sandy ridge systems.     

A GENETIC AND BEHAVIORAL ANALYSIS OF MATE CHOICE AND SONG NEIGHBORHOODS IN INDIGO BUNTINGS

Neighboring males of indigo buntings (Passerina cyanea) share songs in southern Michigan. We sampled polymorphic enzymes to compare the genetic variation between mates and the variation among contiguous song neighborhoods. Mate choice was independent of the genetic and morphometric similarity of female and male, and these measures were independent of each other. The incidence of extrapair copulations and fertilizations was independent of the song of cuckolding males. Breeding success of the mated pairs was independent of their genetic or morphological similarity. Males characterized by different song dialects did not differ in mean lifetime reproductive success. We found no significant genetic differences among the neighborhoods. Most birds that bred in one song neighborhood were born in another, and neighborhoods were not isolated demes. Bunting songs may provide no information to a female about genetic quality of males. The results are consistent with a neutral model of no mate choice for genes.