The Condor 99:413-423 0 The Cooper Omitholog~cal Soaety 1997

CULTURAL EVOLUTION IN THE EURASIAN TREE SPARROW DIVERGENCE BETWEEN INTRODUCED AND ANCESTRAL POPULATIONS ’

ANTHONY L. LANG* AND JON C. BARLOW Departmentof Zoology, Universityof Toronto, 25 Harbord St., Toronto, Ontario, Canada, M5S 3G5 und Centrefor Biodiversityand ConservationBiology, Royal Ontario Museum, IO0 Queens’ Park Cres., Toronto, Ontario, Canada, M5S 2C6, e-mail: [email protected]

Abstract. We investigatedcultural evolution in the song of the introducedNorth Amer- ican population of the Eurasian Tree Sparrow (Passer montanus),derived from 12 pairs broughtfrom Germany in 1870. These birds were liberatedat St. Louis, Missouri, and spread into Illinois. Cultural evolution is described here in terms of the processesof population differentiation where the song meme was the unit of transmission.The distributionof song syllable memes in each meme pool fit a null hypothesisof a neutral model with an equilib- rium between mutation, migration, and drift, indicating that the memes are functionally equivalent. The introduced and ancestral(German) populationsshowed marked divergence in the level of meme sharing. The small size of the founding North American population, the loss of genetic diversity there, and the relative susceptibilityof meme pools to founder effects suggestthat much of the reduction in sharing of syllable types occurred during the founding event. Becausememes also are susceptibleto extinction due to drift, memes were probably lost in both populations as a result of random memetic drift. Meme diversity in Illinois was comparablewith that in Germany, suggestinga large mutational input into the former population following its founding. Estimatesof mutational divergence based on the frequencies of song memes in meme pools showed more population structure in Illinois than in Germany. There also was less meme flow among meme pools in Illinois than in Germany. These results suggest that there were a series of founding events during the colonization of North America. Key words: Eurasian Tree Sparrow, Passermontanus, song, cultural evolution,memetic diffeientiation.

INTRODUCTION Populations introduced by humans are of in- Studies of population differentiation often at- terest to students of evolutionary biology be- tempt to determine the relative importance of the cause they are isolated from the homogenizing various forces that cause and prevent population effect of the flow of genetic and cultural traits divergence. There is considerable interest in de- from the parent population. Because the date of termining the genetic importance of one of these introduction, the size, and the origin of such forces in particular: founder effects and their as- populations often are precisely known, infer- sociated bottlenecks and drift. Theory suggests ences also can be made about the impact of mi- that bottlenecks affect pools of cultural traits in croevolutionary forces on these populations. Al- ways that are analogous to their effects on gene though such introductions are relatively recent, pools (Mundinger 1980, Cavalli-Sforza and high rates of cultural mutation allow cultural Feldman 1981, Lynch and Baker 1993). In fact, evolution to proceed even over short time inter- bottlenecks often have been suggested as the vals (Jenkins 1978, Ince et al. 1980, Lynch et cause of macrogeographicvariation in bird song al. 1989). To date, few studies have examined (Thielcke 1973, Baptista and Johnson 1982, differentiation in song between introduced and Lynch and Baker 1994). However, bottlenecks parental populations of birds (Jenkins and Baker in bird song rarely have been documented in nat- 1984). ural populations (Baker and Jenkins 1987). The Eurasian Tree Sparrow Passer montanus (hereafter referred to as Tree Sparrow) is an ide- al organism with which to study the applicability ’ ’ Received 10 June 1996. Accepted 21 January of models of cultural evolution to bird song. 1997. ZCurrent address:5 Massey Square,Suite 2016, To- This species is native to much of Europe and ronto, Ontario, Canada, M4C 5L6, e-mail: Asia, and was introduced into North America [email protected] when 12 pairs from Germany were released on

14131 414 ANTHONY L. LANG AND JON C. BARLOW

25 April 1870 at Lafayette Park, St. Louis, Mis- and Barlow 1987). The Tree Sparrow is semi- souri (Widmann 1889, Phillips 1928). The small colonial (Summers-Smith 1988) and the territory size of the founding population suggeststhat a defended by males is limited to the nest hole strong potential existed for founder effects to in- (Lang, unpubl. data). The nest-site song is used fluence this population. This hypothesis is sup- only in mate attraction. Males use a visual dis- ported by St. Louis and Barlow (1988) who play (termed Kopfhoch-Drohen or head-up found a reduction in genetic variation in the in- threatening by Deckert 1962) rather than vocal- troduced population. izations to repel other males that venture too Lang and Barlow (1987) discussed evidence close to the nest hole (Lang, unpubl. data). for song learning in the Tree Sparrow and in the House Sparrow (P. domesticus). Cultural trans- SAMPLING mission of song in the Tree Sparrow also is sug- Tree Sparrow nest-site songs were recorded in gested by the extensive variation found in song the breeding season from April to July 1985 in elements among the repertoires of individual Illinois near White Hall, Greene County (WH), males and populations of Tree Sparrows (Lang Beverly, Adams County (BV), Meredosia, Mor- and Barlow 1987). Although cultural transmis- gan County (ME), and Jacksonville, Morgan sion of song has not been studied in detail in the County (JA) (see Lang and Barlow 1987), and Tree Sparrow, studies of a variety of species of in 1987 near Brussels, Calhoun County (BF), oscineshave shown that song elements are faith- Loami, Sangamon County (LO), Industry and fully transmitted acrossgenerations, despite oc- Fandon, McDonough County (MC), Havana, casional mutations (Jenkins 1978, Payne et al. Mason County (HV), and again near Beverly, 1988, Trainer 1989). Adams County (Fig. 1). In Germany, songswere In this report, we test the fit of the distribution recordedin 1986 near Bockenem, Niedersachsen of Tree Sparrow song elements to a null model (NS), in Stuttgart (SG) and near Karlsruhe (KA) in which song elements are selectively neutral in Baden-Wtirttemberg, and in 1988 near Haub- and their distribution is due to an equilibrium ersbronn, Baden-Wtirttemberg (HA), and again among mutation, migration, and drift. We also near Bockenem, Niedersachsen (Fig. 1). An ex- describe the pattern of cultural differentiation tensive sampling regime was followed in which that has developed between song pools of the efforts were made to sample the songs of as introduced North American and ancestral Ger- many localities as possible and to sample as man populations. We present data on song syl- large a portion of the songs of each locality as lable sharing, flow, and diversity in the two pop- possible. Therefore, the songs of many males ulations that, given the history of the introduced were taped at each locality. Because males use population, are consistent with the influence of progressively smaller repertoires as their nesting founder effects, drift, and frequent mutations. cycles progress (Lang, unpubl. data), there is MATERIALS AND METHODS large variation in the repertoire sizes obtained from individual males (with a mean of approx- SONG STRUCTURE imately 10 syllable types). However, we as- The Tree Sparrow is a continuous singer (sensu sumed that the distribution of large and small Hartshome 1956). We follow our original de- repertoires was randomly distributed among scription of the structure of the song of this spe- samples obtained from the 12 localities. The cies (Lang and Barlow 1987) in giving the term date of sampling did not affect the distribution syllable to the song elements that make up its of repertoire sizes from each locality because continuous song. While singing, male Tree Spar- Tree Sparrows raise two to three broods per rows group syllables into bouts that last as long breeding season in North America (Anderson as 10 min. Our operational definition of a bout 1978) and males in the early stageof the nesting is a group of syllables separatedfrom adjacent cycle are present throughout the breeding sea- groups by a time interval of greater than 2.5 set son. Singing males were tape recorded until well (Lang and Barlow 1987). Each male has a rep- after they began to repeat syllable types used in ertoire of as many as 54 distinct syllable types earlier song bouts. Sample sizes are given in Ta- that it uses in the nest-site song. Many of these ble 1. Recordings were made with a Uher 4000 syllable types are sharedwith other males (Lang Report IC tape recorder set at a tape speed of CULTURAL EVOLUTION IN THE EURASIAN TREE SPARROW 415

ILLINOIS GERMANY

U.S. RANGE

0 200 km FIGURE 1. Map showing sampling localities. See text for explanation of acronyms.

19 cm set-l or a Sony WM-D6C tape recorder with a Dan Gibson P-200 parabolic microphone.

ANALYSIS AND DEFINITIONS TABLE 1. Number of birds tape recorded, syllables, Audiospectrograms of songs were made using a syllable types, and private syllable types by locality Kay Elemetrics Sona-Graph 7800 using a wide- and population. band (300 Hz) setting and a frequency range of 80-8,000 Hz, a Unigon FFT Spectrum Analyzer, NO. NO. private and a Kay 7900 printer or a Kay DSP Sona- NO. Total no. syllable syllable Locality birds syllables types types Graph 5500 and Kay 5510 printer. Germany The sharing of syllable types among samples NS 44 380 203 78 served as the basis for assessing the cultural di- KA 57 430 179 66 vergence of the introduced North American pop- SG 58 536 204 68 ulation from the German population. Lang clas- HA 33 327 158 65 sified syllables into syllable types by visual as- Total 192 1,673 503” 360b sessmentof their similarity (Marler and Pickert Illinois 1984, Slater et al. 1984, Lynch et al. 1989), and BF 33 298 141 60 a pool of syllables was developed for each of WH 37 292 169 50 the localities. Syllables were classified so that BV 35 353 140 42 ME 58 346 162 45 there was less variation within than among syl- JA 41 289 154 48 lable types. Figure 2 illustrates this discontinu- LO 299 139 61 ous variation in syllable morphology. Six similar MC 18 210 84 32 syllables from five localities in Germany and Il- HV 44 312 144 59 linois are shown. These syllables were classified Total 295 2,399 697” 554c into two syllable types. Lynch and Baker (1986, Grand total 487 4,072 1,057” 143d 1994) and Lang and Barlow (1987) discuss the ” Syllable types occurring in more than one locality are included only advantages of visually classifying songs over once I” totals. h No. syllable types found m one or more German samples. other methods. Birds also perceive song ele- c No. syllable types found m one or more Illinois samples. *Number of syllable types shared between lllinon and Germany. ments as falling into discrete categories; even 416 ANTHONY L. LANG AND JON C. BARLOW

49Ai syllable or a group of linked syllables. Here we use the term meme to refer only to individual 6 syllables. We refer to the pool of syllables sam- kHz pled from a locality as a meme pool (Lynch et 4 al. 1989). 5r 4 POPULATION DIFFERENTIATION b c The degree of differentiation among meme pools B within a population can be estimated using a 50Di measure of mutational divergence (Lynch and 6 1 Baker 1994). Latter (1973) defined this measure kHz as: 4 h y = 1 - (ZBZIW), (1) b c where Z, is the expected probability of identity I among genes or memes drawn from different 0.1 see gene (meme) pools within that population, and FIGURE 2. An example of the classificationof Eur- I, is the expected probability of identity of asian Tree Sparrowsyllables into syllabletypes with genes (memes) within a gene (meme) pool. less variation in syllable morphology within than Identity here is the probability that two random- among syllable types. A. Syllable type 49Ai. a. male no. M242, locality JA. b. male GM157, locality HA. ly chosen memes are identical. y is dependent c. male M77, locality ME. B. Syllable type 50Di. a. upon mutational input and migration, but is in- male GM2, locality SG. b. male M240, locality JA. c. dependent of sample size in an island model of male GM 120, locality NS. population structure and under a neutral model of differentiation (Lynch and Baker 1994). In an island model, migration is possible between any elements that are continuously varying are cat- pair of gene (meme) pools. The probabilities of egorized (Nelson and Marler 1989). In total, identity were calculated from the frequencies of 4,072 syllables from 487 birds from four Ger- memes in each meme pool (see Lynch and Ba- man and eight Illinois localities were classified ker 1994 for equations). Mutational divergence into 1,057 syllable types. The large number of of song syllables was calculated for both the Il- syllable types and the small mean number of syl- linois and German populations. All calculations lables per syllable type that resulted from this were performed using a Turbo Pascal program classification are a result of three phenomena: written by A. Lynch. (1) males of this species each have large reper- The percentage of syllable types shared toires of syllable types, (2) high rates of cultural among samples was used to examine the rela- mutation generate a large diversity of syllable tionships among the meme pools representedby types (Lynch et al. 1989, Lynch and Baker these samples. A multivariate measure of dis- 1994), and (3) some males sang a small portion similarity (memetic distance) among meme of their repertoireswhen they were taped. There- pools was calculated following Lynch and Baker fore, the sampled repertoires of some of these (1994). The presence(1) or absence (0) of a syl- males shared few syllable types with repertoires lable in the meme pool of a locality was scored, sampled from other males. Numbers of syllables resulting in a binary matrix. Jaccard’scoefficient and numbers of syllable types found in each lo- (Sneath and Sokal 1973) was used to calculate cality are reported in Table 1. The numbers of the level of syllable sharing among meme pools. syllable types restricted to only one sample also The resulting similarity values were converted are listed. These are analogous to “private” al- into distance measures (memetic distance) by leles (Slatkin 1985) and thus are termed private taking their negative natural logs. Memetic dis- syllable types. tances then were used to reconstruct the rela- We follow Dawkins’ (1976) use of the term tionships among meme pools. Neighbor-joining meme for any culturally transmittable trait, and (Saitou and Nei 1987) and UPGMA cluster anal- Jenkins and Baker’s (1984) definition of song yses, principal coordinate analysis, and multi-di- meme as a culturally transmittable individual mensional scaling (Sneath and Sokal 1973) were CULTURAL EVOLUTION IN THE EURASIAN TREE SPARROW 417 performed on these distances using the NT-SYS (see Lynch and Baker 1993 for equation). & is package of statistical programs (Rohlf 1988). A here termed the effective number of memes. & minimum spanning tree was calculated using represents the number of different memes that NT-SYS to connect the samples in principal co- would exist in an ideal population in which all ordinate space. memes have equal frequency. The value of $ can range from 1 (only one meme) to a value ESTIMATES OF MEME FLOW equal to the number of memes in the population Meme flow among meme pools within each of (an even frequency distribution) (Lynch and Ba- the two populations (Illinois and Germany) was ker 1993). Confidence intervals of diversity es- estimated using Slatkin’s (1985) rare alleles timates were calculated using the delete-half method. This method uses the frequencies of al- jackknife resampling procedure (Wu 1986). A leles restricted to one gene pool (“private” al- frequency distribution of diversity estimateswas leles) to indicate gene flow. The method as- obtained and the 2Sth and 97Sth percentiles sumes that these frequencies will be high when were used as the 95% confidence limits. For the level of flow among gene pools is low and each sample, 1,000 replicates were performed. that they will be low when the level of flow is Both $ and the confidence intervals were cal- high. Lynch et al. (1989) showed that this meth- culated using a Turbo Pascal program written by od can be applied to bird song memes. Flow is A. Lynch. calculated using the formula: TESTS OF NEUTRALITY l@(l)] = a[ln(Nm)] + b, (2) The distributions of song elements in popula- where z?(1) is the mean frequency of alleles (me- tions of several species of birds conform to a mes) restricted to one gene (meme) pool, and a neutral model (Slater et al. 1980, Lynch and Ba- and b are constants(Slatkin 1985). The resulting ker 1993, Lynch 1996). This suggeststhat the value of Nm is an estimate of the number of distributions of memes in these species are not genes (memes) per generation that are derived due to selection but to random processes.To test from migrants. the neutrality of memes in the Tree Sparrow, we used Lynch and Baker’s (1993) method to com- MEME DIVERSITY pare the observed distribution of meme frequen- Meme diversity of sampleswas calculated using cies with the distribution expected in a neutral, the method of Lynch and Baker (1993). They infinite alleles model. Lynch and Baker (1993) applied the Kimura and Crow (1964) infinite al- used Ewens’ (1972) maximum likelihood meth- leles model to memes, in which memes belong od to generatethe expecteddistribution of meme to a single locus with infinite alleles. The model frequencies. Ewens (1972) showed that this dis- assumesthat each mutation creates a new meme tribution could be estimated from the total num- that is different from previous memes. Given the ber of distinct memes, s, in a sample and the large number of memes found in Tree Sparrow size of the sample, n. Following Watterson song samples (Table l), the probability that two (1978), Lynch and Baker (1993) compared the memes (syllables) are similar due to conver- observed and expected values of I to test the fit gence is probably low, especially when the short of the observed distribution of meme frequen- time that the German and Illinois populations cies to that expected under a neutral model. The have been separatedis taken into consideration. observed value of Z can be calculated as above, Therefore, this model seemsappropriate. To cal- and the expected value can be obtained using culate meme diversity, Lynch and Baker (1993) the equation: used an estimate of meme identity from popu- E(Z) = l/(8 + l), lation genetics and calculated its inverse. The (4) resulting value is known as the effective number where 0 = 2N,v and is derived from Ewens’ of alleles (Kimura and Crow 1964): (1972) maximum likelihood method (Lynch and Baker 1993). v is the combined effect of muta- ,. = l/i, s, (3) tion (p) and migration (m) rates. Lynch and Ba- where i is an unbiased estimate of meme iden- ker (1993) calculated the expected values of Z tity. Identity estimates were calculated from the by simulation and obtained confidence limits frequency of each syllable type in each sample from the resulting distribution. We calculated the 418 ANTHONY L. LANG AND JON C. BARLOW

TABLE 2. Among-meme pool differentiation (y), The results of the principal coordinate analy- mean frequency of private syllables @ [ 11) and stan- sis are shown in Figure 3. This analysis was dard error (SE), and estimates of meme flow (Nm) among meme pools. based on memetic distances (Table 3). The first three axes accounted for 61.6% of the variation

Population Y P (1) fSE Nm (axis 1: 34.4%, axis 2: 14.8%, axis 3: 12.4%). Illinois 0.767 0.00599 50.00022 34.03 The plot shows a greater degree of sharing of Germany 0.689 0.00461 ~0.00021 87.83 syllable types among meme pools within the pa- rental and introduced populations than between the two populations. The divergence between observed and expected value of Z for each of the the two populations was so great that few syl- samples using a Monte Carlo simulation per- lable types are presently shared (Table 1). The formed by a Turbo Pascal program written by eight Illinois meme pools separated from the A. Lynch. four German meme pools on the first axis of the principal coordinate analysis. Although Illinois RFSUL.TS and German meme pools are not separated on POPULATION DIFFERENTIATION AND MEME the second and third vectors, the minimum span- FLOW ning tree suggests that the Illinois meme pools The two populations differed in their degree of are most similar to each other and that each Ger- population structuring. There was more muta- man meme pool is most similar to other German tional divergence among the Illinois meme pools meme pools. Multidimensional scaling gave a than among the German meme pools (Table 2). similar result. Levels of meme flow among meme pools were Results of cluster analysis of memetic dis- consistent with levels of differentiation, being tances were similar to those from the principal lower among meme pools in Illinois than in Ger- coordinate analysis. Figure 4 shows the results many (Table 2). of clustering using the neighbor-joining method,

FIGURE 3. Three-dimensional principal coordinate solution and minimum spanning tree based on memetic distances among Illinois and German meme pools. Closed circles represent samples of memes from Illinois localities and open circles are samplesfrom German localities. See text for explanation of acronyms. CULTURAL EVOLUTION IN THE EURASIAN TREE SPARROW 419

TABLE 3. Memetic distancesamong German and Illinois samples.

KA NS HA SG WH JA ME BV BF HV LO Karlsrnhe Niedersachsen 1.622 Haubersbronn 2.155 1.759 Stuttgart 1.625 1.589 1.720 Whitehall 3.100 2.767 2.786 2.511 Jacksonville 2.601 2.879 2.736 2.547 ,458 Meredosia 2.627 2.610 2.558 2.312 ,488 1.390 Beverly 2.941 2.680 2.937 2.785 ,822 2.002 1.742 Brussels 2.708 2.546 2.748 2.593 2.350 2.295 2.325 2.371 Havana 2.890 3.030 2.819 2.648 2.072 2.153 2.047 2.295 2.697 Loami 3.006 2.677 2.934 2.730 2.303 2.561 2.492 2.458 2.414 2.425 McDonough 2.737 2.898 2.953 3.136 2.511 2.389 2.321 2.565 2.327 2.653 2.703

and reveals divergence between Illinois and Ger- German meme pools (Fig. 4). When untransfor- man meme pools. UPGMA gave results that med memetic distances were used in various or- were virtually identical in topology to those dination and clustering methods, virtually iden- from the neighbor-joining method, but because tical results were obtained. the neighbor-joining method does not assume equal rates of evolution on all branches, only MEME DIVERSITY results from the latter are illustrated. Identical trees were obtained whether the tree was rooted In general, meme diversity in Illinois meme at the midpoint or using the German meme pools pools was not significantly different from that of as outgroups. This tree shows slightly longer German meme pools, despite some variation in branch lengths for the Illinois meme pools than diversity estimates among the meme pools. This

115 110 0.5 A

Memetic Dis+anc’i FIGURE 4. Neighbor-joining cluster analysis of memetic distancesamong Illinois and German meme pools (cophenetic correlation: r = 0.82, P = 0.001). 420 ANTHONY L. LANG AND JON C. BARLOW

40 lLLlN0l.S GERMANY

FIGURE 5. Meme diversity by meme pool, where meme diversity is measured by the effective number of memes (5); see text for details. is illustrated by overlap in 95% confidence limits vergence is probably largely due to founder ef- (Fig. 5). fects as suggestedby the small size of the found- ing population, genetic evidence (St. Louis and TESTS OF NEUTRALITY Barlow 1988), and cultural evolutionary theory There was good agreement between the ob- (Cavalli-Sforza and Feldman 1981, Lynch and served and expected values of Z in each of the Baker 1994). Although St. Louis and Barlow meme pools (Table 4). This suggests that within- (1988) did not detect a reduction in mean het- meme pool variability was primarily neutral and erozygosity in the Illinois population, they found that the distribution of memes is a result of input a small but statistically significant reduction in from immigration and mutation and elimination the mean number of allozyme alleles per locus of memes due to random extinction. (St. Louis and Barlow 1991). Experimental ma- nipulation of population size in fish by Leberg DISCUSSION (1992) showed that the latter is a more sensitive The meme pools of the North American popu- indicator of bottlenecks. St. Louis and Barlow lation of the Tree Sparrow have diverged con- (1988) attributed the reduction of genetic diver- siderably from those of the German population. sity in the Illinois population to founder effects This divergence is manifested in the dramatic and genetic drift as a result of the small size of loss of shared syllable types in the 115 years the founding population. Therefore, there was a between the introduction of this speciesto North high potential for the meme pool to have under- America and our sampling (Table 1). This di- gone founder effects and drift as well. A loss of syllable types as a result of founder effects would account for the observed lack of syllable TABLE 4. Observed (fi and expected [E(Z)] meme type sharing between Illinois and Germany. Re- identity within meme pools. sults from cluster analysis using the neighbor- joining method suggest that drift immediately Locality I WI 95% CL following the founding event also had an impact NS 0.0050 0.005 1 0.0043-0.0064 on the Illinois population. Longer branch lengths KA 0.0074 0.0076 0.0059-0.0105 SG 0.0080 0.0085 0.0069-0.0101 for Illinois meme pools suggest more rapid di- HA 0.0078 0.0078 0.0063-0.0101 vergence as a result of drift than in Germany BF 0.0086 0.0094 0.0073-0.0176 (Fig. 4). Despite drift in the parental German WH 0.0056 0.0063 0.005 l-O.0077 population, a loss of syllable types of the same BV 0.0099 0.0113 0.0090-0.0195 ME 0.0074 0.0087 0.0069%0.0107 magnitude probably did not occur there because JA 0.0068 0.0078 0.0062-0.0092 of replenishment of lost syllable types via meme LO 0.0084 0.0099 0.0079-0.0133 flow from adjacent European populations. The MC 0.0155 0.0193 0.0143-0.0283 action of drift on bird song has been implicated HV 0.0104 0.0099 0.0075-0.0125 by other studies of isolated populations of birds CULTURAL EVOLUTION IN THE EURASIAN TREE SPARROW 421

(Bitterbaum and Baptista 1979, Baker and Jen- then 10 per cent of the meme pool would be kins 1987, Lynch and Baker 1994). composed of that syllable type. This represents The divergence between the Illinois and Ger- the maximum percentage that could be attained man populations also is probably characterized by a syllable type in this sample. Because many by the creation of a large number of syllable syllable types are not shared by all males in types due to mutation. Both the finding that lev- samples of Tree Sparrow song, such syllable els of diversity in Illinois are comparable with types have even lower frequencies. For example, that of Germany and the presence of a large in the WH meme pool, syllable types range from number of private syllable types in the Illinois 0.3 to 2.4% of the sample with a mean of 0.6%. population (Table 1) suggest that a high muta- In contrast, most allozyme loci in Tree Sparrow tion rate restored diversity in Illinois. This find- samples have only one or two alleles, and there- ing is consistent with Lynch and Baker’s (1994) fore most alleles are not rare (St. Louis and Bar- prediction that meme diversity would rapidly re- low 1988). Founder effects acting on such sam- cover following a founding event due to the high ples would result in the loss of only the few rare mutation rates that have been observed for me- alleles, but many syllable types. Syllable types mes (Jenkins 1978, Slater and Ince 1979, Lynch also probably are prone to extinction due to drift and Baker 1994). Together, these results, as well for the same reasons that they are easily lost to as the loss of genetic variation in the Illinois founder effects (Lynch et al. 1989, Lynch and population, suggest that the divergence of Illi- Baker 1994). nois meme pools from German meme pools was The present results suggest that the Illinois due primarily to both the loss of a large number population also differs from the German popu- of syllable types during the founding of the Il- lation in that colonization events in the intro- linois population and to a large mutational input. duced population appear to have resulted in Our results are consistent with theory that greater population structuring in Illinois than in suggeststhat syllable types are highly suscepti- Germany. Although levels of meme diversity in ble to loss due to founder effects. This is a result Illinois meme pools are comparable with those of syllable types generally occurring at low fre- of meme pools in Germany, there is less sharing quencies and subsequently having very high di- of syllable types among meme pools in Illinois versity (Lynch et al. 1989, Lynch and Baker than in Germany. This is reflected in a greater 1994). These low frequencies also are evident level of mutational divergence (y) and lower rate among Tree Sparrow syllable types as can be of meme flow among Illinois meme pools. These seen in Table 1 where the number of syllable results suggestthat there were several founding types is large relative to the number of syllables. events and subsequent drift as small groups of This low average frequency and high diversity birds from the recently founded Illinois popu- arises in part from the large population size for lation colonized new areas, and that there has memes (Lynch et al. 1989, Lynch and Baker not been enough time for meme flow to bring 1994). For example, each male Tree Sparrow levels of syllable type sharing among meme can potentially carry over 50 distinct syllable pools up to those found in Germany. Longer types, as opposed to only two copies of each branch lengths for Illinois meme pools in the gene locus. The high rates of mutation typical neighbor-joining tree may be due in part to such for memes also contribute significantly to the effects. high diversity and hence the low frequencies Bottlenecks in the total size of the North seen for syllable types (Lynch et al. 1989, Lynch American population size following the initial and Baker 1994). Therefore, a small group of colonization event probably did not occur and birds selected to found a population is likely to therefore would not have played a role in the carry syllable types that are representative only reduction in overall syllable sharing between Il- of a very small area of the ancestral population, linois and Germany. The Illinois population ap- whereas their allozymes would be representative pears to have grown rapidly shortly after release of a much larger area. As an example, consider (Merrill 1876, Widmann 1889). As discussed a hypothetical sample of 30 birds each with a above, some Illinois meme pools may have lost repertoire of 10 syllable types. This representsa more syllable types through individual founder meme pool size of 300 syllables. If each of these effects and drift than did German meme pools. 30 males sang a copy of the same syllable type, However, these syllable types were likely pres- 422 ANTHONY L. LANG AND JON C. BARLOW ent in other Illinois meme pools. This would also are important. These can corroborate the have prevented further net reduction in syllable findings of the indirect methods used here. sharing with Germany. Although testing of al- ternative hypotheses to explain the divergence ACKNOWLEDGMENTS of Illinois and German meme pools was beyond We thank A. Lynch, R. B. Payne, D. R. Kozlovic, D. the scope of this study, two hypotheses would W. Dunham, R. I. C. Hansell, and J. D. Rising for their be worthy of investigation. Lynch and Baker comments on earlier drafts of this manuscript,and D. (1993) suggestedthat colonization by juveniles Jackson and A. Lynch for statistical advice. We also that have not completed song learning (“with- thank the many people who helped us in field work: in Illinois, J. and T Barlow, E Bellrose, H. Draayer, drawal-of-learning;” Thielcke 1969, 1973) E. Frank, E., J., L., and M. Funk, G. T. Girard, A. and could cause an initial reduction in meme diver- B. Henry, R. Randall, Mrs. Sparks, T Ward, M. Wat- sity in a founding population. However, Illinois son, G. White, and especially I? Ward; in Germany, B. meme pools shared approximately 14% of their and M. Herrmann, R. Lamprecht, A. Papenfoth, K. Ruge, A. Schltiter, and especially H. Dannenmayerof syllable types with German meme pools and the the Vogelschutzwartein Karlsruhe and C. Kiinig of the remaining Illinois syllable types are similar to Staatliches Museum fur Naturkunde in Stuttgart. We German syllable types, suggestingthat the foun- thank the staff of the University of Toronto Zoology ders of the Illinois population had learned the Department and the Royal Ontario Museum Centre for species typical song. There may be differences Biodiversity and Conservation Biology for assistance with electronic equipment,AV, and library matters:M. in the acoustical environments of Illinois and Austerberry, S. Cooper, K. Gallant, 0. Haddrath, N. Germany that also could have an impact on the Hatton, E.-Knapp, H. Meyer, S. Smith, and W. Thiel. composition of meme pools. However, the hab- These studieswere SUDDOitedbv an NSERC Posterad- itat occupied by Tree Sparrows in the two areas uate Scholarshipand cniversity of Toronto Open-Fel- lowships to A. L. Lang and by NSERC grantsawarded at the present time appearssimilar. In both areas, to J. C. 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