Evolutionary Ecology, 1996, 10, 375-385

Colonial breeding and speciation in birds

A R N E 0 . M O O E R S 1. and A N D E R S P A P E M O L L E R 2 tDepartment of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK 2Zoological Institute, Copenhagen University, Universitetsparken 15, DK-2100, Copenhagen ¢), Denmark

Summary

It was recently suggested that bird species which breed colonially might be under stronger sexual selection, have faster rates of evolution and might therefore speciate more rapidly than bird species which do not. If true, then colonial taxa should contain more species than non-colonial taxa, other things being equal. When similarity through common descent is accounted for, there is little evidence for an association between the number of species in a clade and whether it is colonial or not.

Keywords: Ayes; coloniality; speciation; diversity

Introduction

In 1992, Birkhead and MOiler published a novel hypothesis linking colonial breeding to increased rates of diversification in birds (Birkhead and M0ller, 1992, pp. 246-7; see also Marzluff and Dial, 1991). Their hypothesis stemmed from comparative evidence which showed that birds living in colonies had increased rates of extra-pair copulations (EPCs) than did birds with other breeding systems (Wittenberger and Hunt, 1985; Birkhead and M011er, 1992; M011er and Birkhead, 1992) and that fewer males took part in EPCs than did females (M011er and Birkhead, 1993). It follows that colonial birds may have smaller effective population sizes and, hence, more rapid rates of evolution (Wilson, 1975; Bush et al., 1977). ff females are choosing both their mates and the males engaging in EPCs based on heritable cues correlated with fitness, then colonial populations may be better able to track environmental changes and show increased adaptability (Birkhead and M011er, 1992). If adaptations are local, then the effects of small population sizes and of sexual selection (see Lande, 1982; Schluter and Price, 1993) could lead to more rapid speciation. In addition, the ability to respond quickly to changing local conditions might increase the longevity of colonial species, thereby increasing the chance of speciation.

Taken together, these observations suggest that colonial taxa should contain more species than non-colonial ones. We tested this hypothesis using a variety of novel methods and the systematic works of Sibley and Monroe (1990) and Sibley and Ahlquist (1990).

Methods and data

Methods

Historically, three approaches have been taken in identifying associations between traits and taxonomic diversity. The first is simply to identify a trait shared by members of a speciose clade (the 'key innovation'; see the review by Heard and Hanser, 1995) and then to make a plausibility argument for its effect on the rates of effective cladogenesis (e.g. mantle fusion in bivalves: Stanley, 1979). The second is the taxon correlational approach, which compares the diversity and

* Address all correspondence to Arne O. Mooers, Department of Zoology, University of British Columbia, Vancouver, B.C. V6T 1Z4, Canada,

0269-7653 © 1996 Chapman & Halt

376 Mooers and M¢ller

trait values of several clades of the same rank (e.g. body size and diversity of bird families: Kochmer and Wagner, 1988; Nee et al., 1992). The third method is sister group comparison, where sister clades that differ in the trait under test and in diversity are compared with each other in a test of association (e.g. latex and resin canals in plants; Farrell et al., 1991). None of these methods is ideal. Briefly, there is no way of being confident that the trait picked out as the putative 'key innovation' leading to diversification is the right one (Lander, 1981). The taxon correlational approach is hampered by the fact that most taxa of equal rank are neither monophyletic nor of similar age and are not independent data points (Cracraft, 1984). Finally, the sister group comparison approach, which holds the most promise, has, until recently, been considered overly conservative, allowing only a sign test (Heard and Hauser, 1995).

Recently several investigators have suggested refinements of the sister group approach (Slowinski and Guyer, 1994; S. Nee, personal communication). Drawing on earlier work (Farris, 1976; Slowinski, 1990), Slowinski and Guyer (1994) pointed out that under a null model where the probability of speciation (and extinction) is random and equal for all lineages at any one time (an equiprobable Markov model of tree production), all possible subdivisions of n species between two sister groups of size r and n - r are equally likely. This allows a simple formula for the cumulative probability that a sister group exhibiting some trait hypothesized to increase diversification will have at least r number of species, given that the two sister groups together have n species: Pc(rln) = (n-r) /(n-1) . The sign test can now be extended, as each sister group comparison can be assigned a separate probability and a Fisher's combined probability test (Sokal and Rohlf, 1981) performed. This model-based sister group comparison technique would seem well suited for clearly defined qualitative traits (e.g. phytophagy in insects, breeding systems in birds and the presence or absence of mantle fusion).

Nee et al. (in press) point out that Slowinski and Guyer's (1994) test would allow a statistically significant statement about a correlate of diversification to be made on the basis of a single bifurcation (e.g. a group with n = 21 species and r = 20 species would produce p = 0.05). Similarly, a large number of small sister group comparisons (e.g. with n = 3 and r = 2, such that p = 0.5) would never produce a statistically significant statement when considered in a Fisher's ×2 test.

Nee et al. (in press) propose a randomization approach which can be used to test for a correlation between a given trait and species richness. Consider a sister group comparison with n total species split into groups having r and n - r species. Under the null hypothesis, it is equally likely that the group exhibiting the trait under test has r or n - r species. If we express each comparison as the proportion of species in the sister clade that exhibits the trait under test, the expectation of that ratio under the null hypothesis will be 0.5 (the mean of r/n and (n-r)/n). The sum of all such ratios (one for each comparison) will have an expectation equal to one-half the number of comparisons. If the trait is associated with large sister clades, the observed ratios will be greater than 0.5 and the sum will subsequently be greater than the expectation. We first calculate the sum for the observed data. We then compare this statistic with sums created by (1) randomly permuting the trait between sister clades, (2) recalculating a new ratio at each sister group comparison and then (3) summing across comparisons. The distribution of these randomized sums will be affected by the actual size differences in the observed sister group comparisons. If the trait is statistically associated with species richness, then the observed sum should be at least as large as the largest 5% of the statistics calculated from the randomizations (for p <- 0.05).

In order to test the colonial breeding hypothesis of diversification, we collected data on breeding dispersion for a number of bird species and performed three analyses. In the first analysis, we assumed monophyly and similar ages for the tribal rank of the Aves, as defined by

Coloniality and speciation in birds 377

Sibley and Monroe (1990) and applied the taxon correlational approach. In the second and third analyses, we made independent comparisons between colonial and non-colonial sister taxa. First, we compared sister clades which differed in both the proportion of colonial species and taxonomic diversity. We then parsimoniously reconstructed ancestral states (colonial and non- colonial) on the UPGMA (unweighted pair group method using arithmetic averages) tree of the birds (Sibley and Ahlquist, 1990) and compared sister clades that differed in their putative ancestral states and taxonomic diversity. We employed the various methods outlined above to see whether colonial taxa were consistently more speciose than their non-colonial sister taxa.

The data

An exhaustive literature search produced data on the breeding dispersion of 2700 species of birds representing 191 tribes as defined by Sibley and Monroe (1990). Species were coded as colonial (including semi-colonial, 'small colonies' and 'clumped' neighbourhood groups) and non-colonial[ (dispersed and territorial) breeding species. A minimum sample of five nest sites was required before a species' breeding dispersion was considered known.

Since body weight is often negatively correlated with the species richness of clades (Van Valen, 1973; May, 1986; Dial and Marzluff, 1988; Kochmer and Wagner, 1988), the body weight for 175 tribes was included in the analysis, reconstructed using Felsenstein's (1985) algorithm. This follows the logic of Harvey and Mace (1982) and eliminates bias from speciose subtaxa. Logarithmically transformed species values were averaged first into generic and then tribal means, using the computer program CAIC (Comparative Analyses Using Independent Contrasts; Purvis and Rambaut, 1995). The program assumes a Brownian motion model of evolution. This model reconstructs the trait value at a higher node as the mean of the values at daughter nodes, inversely weighted by the lengths of the branches from the daughter nodes to the higher node. Because most variation in body size in birds occurs at high taxonomic levels (Bennett, 1986), the reconstructions should be fairly robust with respect to the actual algorithm used. A detailed description of the algorithm can be found in Pagel (1992).

Finally, because the sampling effort across tribes was uneven, the proportion of species surveyed was also recorded and controlled for in the analyses. The data are available on request.

The tribe level of Sibley and Monroe (1990) was chosen as the primary level of analysis. This level, while arbitrary, is a compromise between the family level, systematically stable but containing few data points and the unwieldy number of systematically fluid genera; interesting ecological patterns can be found at the tribal level (Cotgreave and Harvey, 1991, 1994; Nee et alo, 1991). Two measures of tribal coloniality were created - the proportion of species within a tribe censused that were colonial and a parsimony reconstruction of the tribal character state as colonial or non-colonial. The parsimony reconstruction was produced from a coarse working phylogeny created from the explicitly systematic taxonomy of Sibley and Monroe (1990). Species were assigned to genera and tribes with each genus and tribe considered as a polychotomy. Inferred ancestral character states were then assigned to individual genera and tribes using in- group, comparison, under the parsimony assumption of minimizing state changes (Swofford and Olsen, 1990).

Particular statistical tests are described below with their results.

Results

Analysis across tribes

The analysis is based on the 175 tribes for which a representative body size (In(body weight) in grams) and an estimate of the proportion of colonial species were available.

378 Mooers and M¢ller

Table 1. Spearman rank correlation coefficients among tribal values for birds (n = 175)

Number of species % surveyed % colonial

In(weight) - 0.379*** 0.463*** 0.293*** Number of species - 0.645*** 0.127 (p = 0.09) % surveyed 0.291"**

***p < 0.001.

The variables considered were the proportion of the total number of species in the tribe surveyed, the proportion of the species surveyed that were colonial breeders, the number of species in the tribe and the representative body size for the tribe.

None of the four variables was normally distributed. The proportion of colonial species was strongly bimodal, with > 75% of the tribes falling into one of two categories: strongly colonial ( > 80% species colonial) or strongly non-colonial ( < 20% species colonial). Body size and number of species were mildly skewed right and the percentage surveyed strongly skewed left. All the variables were correlated with each other (see Table 1).

The hypothesis being tested predicts a positive correlation between the proportion of species in a tribe that are colonial and the total number of species in the tribe but we need to remove the effect of potentially confounding variables. Because large-bodied clades tend to be both colonial and have few species, body size may obscure any relationship between coloniality and species number. Likewise, because the sampling effort varies positively with the proportion of colonial species in a tribe and negatively with the size of the tribe, large clades will tend to have a lower proportion of colonial species because of the lower sampling effort.

In order to control for body mass and sampling effort, multiple regression was employed (Sokal and Rohlf, 1981). The data for each variable were first transformed by normalizing the ranks. Data for each variable were ranked by size and then for each data point the corresponding value of the normal distribution (Fisher and Yates, 1975) was substituted for the actual value. Normalized data were constructed by taking the means from 100 random samples drawn from a normal distribution with n = 175 (mean = 0, so = 1). Information is lost in this procedure as the actual variance in the dependent variable (number of species) cannot be partitioned among the independent variables. In addition, higher order relationships (e.g. non-linearity) cannot be assessed. However, the levels of significance of the regression of the y-variable on each x-variable can be assessed independently of the other x-variables. Using the normalized data, a multiple regression of species number against mass, the proportion surveyed and the proportion colonial shows that the proportion of colonial species in a tribe is significantly and positively related to the number of species independent of the mass and sampling effort (t-tests of multiple regression coefficients for normalized ranks: mass = 3.04 (p = 0.002), proportion surveyed = 9.03 (p = 0.0001) and proportion colonial = 3.32 (p = 0.0004); n = 175).

Using tribes as independent data, tribes with a higher proportion of colonial species are, indeed, more speciose.

Sister group comparisons

Proportion colonial versus number of species. The branching pattern of the Sibley and Ahlquist (1990) UPGMA (Sokal and Michener, 1958) tree was used to identify sister groups which differed both in what proportion of their species were colonial and in their taxonomic diversity. The maximum number of non-overlapping comparisons was 26. These are listed in Table 2. Tribes with less than 10% of their species colonial were not compared with less colonial taxa. In

Coloniality and speciation in birds 379

Table 2. The 26 independent comparisons of more colonial versus less colonial taxa, based on the UPGMA tree of Sibley and Ahlquist (1990)

Number of species Reconstructed size

Comparison a More colonial Less colonial More colonial Less colonial

Megapodidae versus Cracidae 19 Anserini versus Anatini 43 Anseranatidae versus Anhimidae 1 Lybiidae versus Indicatoridae-Picidae 42 Meropidae versus Cerylidae-Todidae 26 Urocoliinae versus Coliinae 2 Apodidae versus Hemiprocnidae 99 Steatomithidae versus Nyctibiidae 1 Caprimulginae versus Chordeilinae 68 Aramini versus Heliomithini 1 Tringinae versus Scolopacinae 63 Rostratulidae versus Jacanidae 2 Dromadinae versus Glareolinae 1 Larini versus Sternini 50 Pandioninae versus Accipitrinae 1 Pelecaninae versus Balaenicipitinae 8 Ciconiinae versus Cathartinae 19 Hydrobatinae-Diomedeinae versus

Procellariinae 35 Ptilonorhynchidae versus Menuridae 20 Meliphagidae versus Pardalotidae 182 Aratimini versus Oriolini 24 Sturnini versus Mimini 114 Hirundidae versus Regulidae-Sylvidae 87 Estrildini versus Viduini 140 Carduelini versus Drepanidini 136 Icterini versus Cardinalini 97

50 1292 1301 89 2535 975

3 2069 1922 232 39 37

99 35 32 4 66 50 4 28 68 7 407 290 8 49 78 3 1100 355

25 93 166 48 100 114 17 292 84 45 476 141

239 1524 1055 1 6634 5009 7 2981 4093

80 399 408 4 140 90

68 22 11 111 No d~a 45 34 87 48

911 18 13 15 12 20 30 26 18 42 77 32

aColonial versus non-colonial taxon. Groups separated by a dash are the smallest monophyletic clade containing the named taxa. Size is in grams, reconstructed using Felsenstein's (1985) algorithm.

11 o f the 26 comparisons, the larger sister clade also had the higher proportion o f colonial species (two-tailed sign test, p = 0.56). Neither Slowinski and Guyer ' s (1994) test nor Nee ' s randomization test suggested any association between increased coloniality and increased diversity (Fisher 's ×2 (52 d.f.) = 45.2, p = 0.26; Nee ' s randomization test, p = 0.71, n = 1000 randomizations for all tests).

The proportion surveyed, which was a confounding variable in the taxon correlational approach, did not differ between more colonial and less colonial sister clades (in 14 out o f 26 cases the clade with more colonial species was also better sampled: two-tailed sign test, p = 0.85). However , in over twice as many comparisons the colonial clade was also the heavier- bodied clade (17 out o f 25 comparisons: two-tailed sign test, p = 0.11). In addition, lighter sister clades tended to be more speciose (15 cases out of 25, two-tailed sign test, p = 0.42; Fisher 's X 2 (50 d.f.) = 66.69, p = 0.057; Nee ' s randomization test, p = 0.011).

In order to control for the putative effects o f size, a general linear model was constructed to produce a body size-independent measure o f species number. A general linear model (MINITAB,

380 Mooers and M¢ller

release 8.1, Minitab Inc., 1991) of logarithmically transformed species number with a single parameter (body size) explained 22% of the variation and produced well-behaved residuals. This procedure adequately controls for the effects of body weight. However, because groups were considered independent data points, the confidence limits of the model may be artificially low (see Pagel (1993) for a discussion). These residual In(species numbers) were then back transformed to a corrected species number by first adding a constant to each residual and then taking the anti-log such that the range of corrected species numbers paralleled the original data. The corrected numbers were then substituted for the actual species numbers. Sister group comparisons with the corrected species numbers did not suggest an association between species richness and taxonomic diversity (12 of 25 comparisons showed the relationship, two-tailed sign test, p = 1.00). Nee's randomization test, which is valid for corrected species numbers, did not suggest any relationship (p = 0.47).

Parsimony reconstructions. All 191 tribes were first designated as ancestrally colonial (31 tribes), non-colonial (155 tribes) or equivocal (five tribes) based on in-group comparison. The UPGMA tree was then used as an estimate of phylogeny above the tribal level. The states at nodes above the tribal level were estimated using Fitch (1971) parsimony. Different rules for assigning character states at equivocal nodes (ACCTRAN and DELTRAN; Swofford and Maddison, 1987) did not change the set of possible comparisons on the tree.

From the reconstructions, 13 independent comparisons between colonial and non-colonial sister clades were possible (see Table 3); one further comparison, between the Recurvirostrini and the Haematipodini, was uninformative (both clades contain 11 species).

Only four of these comparisons supported the hypothesis that the colonial clade contains more species (×2 (26 d.f.) = 21.08, p = 0.74; Nee's randomization test, p = 0.87).

There was no systematic difference between the sister clades in body mass. In eight out of 12 cases where body mass differed, the colonial sister clade was heavier (two-tailed sign test, p =

Table 3. The 13 independent comparisons of colonial versus non-colonial taxa, based on a parsimony reconstruction of coloniality on the UPGMA tree of Sibley and Ahlquist (1990)

Number of species Reconstructed size

Comparison a More colonial Less colonial More colonial Less colonial

Anseranatidae versus Anhimidae 1 Apodidae versus Hemiprocnidae 99 Steatornithidae versus Nyctibiidae 1 Aramini versus Heliomithi 1 Ropstratulidae versus Jacanidae 2 Recurvirostrini versus Haematipodini 11 Dromadinae versus Glareolinae 1 Pandioninae versus Accipitrinae 1 Pelecaninae versus Balaenicipitrinae 8 Ciconinae versus Cathartinae 19 Hydrobatinae-Procellarinae versus

Gaviidae 115 Bombicyllidae versus Cinclidae-Turdidae 8 Hirundidae versus Regulidae-Sylvidae 89 Ploceinae versus Estrilidinae 117

3 2100 1920 4 28 68 7 400 290 3 1100 355 8 100 117

11 230 640 17 290 84

239 1525 1055 1 5010 6634 7 2980 4090

5 3160 380 602 35 35 911 18 13 155 26 13

aColonial versus non-colonial taxa. Groups separated by a dash are the smallest monophyletic clade containing the named taxa. Size is in grams, reconstructed using Felsenstein's (1985) algorithm.

Coloniality and speciation in birds 381

0.38). Interestingly, for ten of the 12 sister group comparisons, a smaller body size was associated with increased diversity (two-tailed sign test, p = 0.038; Fisher ×2 (24 d.f.) = 44.91, p = 0.026; Nee's randomization test, p = 0.015).

Body size was controlled for as before. A model with the two terms In(mass) and (In(mass)) 2 explained 47% of the variation in In(species number) and produced well-behaved residuals. Only five of the sister comparisons showed an association between the colonial breeding and the corrected number of species (two-tailed binomial test, p = 0.58; Nee's randomization test, p = 0.79). Even after correcting for the putative effects of body size, there seems to be no association between colonial breeding and increased divesity.

Discussion

The evolution of coloniality has been difficult to explain because of the large number of apparent costs associated with it (Hoogland and Sherman, 1976; Birkhead and MOiler, 1992) and has historically been considered a response to unpredictable and patchy food resources (Lack, 1968). One consequence of coloniality is the increased potential for EPCs (Morton et al., 1990; Birkhead and M011er, 1992; Wagner 1993). Moiler and Birkhead (1992, 1993) presented evidence that both the frequency of EPCs and the proportion of females which have EPCs are relatively higher in populations and species of colonial breeders than in their non-colonial close relatives. Birkhead and MOiler (1992) also showed that the percentage of extra-pair paternity is positively related to the percentage of EPC. This suggests the possibility of a large variance in male mating success in colonial species. As expected, Barrowclough (1980) offered some evidence that colonial species of birds have higher levels of population-level genetic variance (FsT; Wright, 1978) than non-colonial species. Colonial breeding brings with it a suite of selective pressures including high levels of parasitism (Brown and Brown, 1986), which are thought to be strong selective agents (Hamilton, 1982). The observed levels of population-level diversity could be due to the rapid evolution of traits which are locally adaptive, for example resistance to local parasites.

This process of local adaptation will be strengthened if females are choosing mates based on heritable cues and the choices are consistent across generations. If there is a restricted gene flow between populations, mate choice based on heritable cues will further decrease the effective population size. Rapid local evolution can lead to rapid divergence and, hence, increased rates of speciation. The heritable cues used could be due to Fisherian runaway sexual selection (Fisher, 1930; Lande, 1982; see also Bakker 1993) or to honest signals of 'good genes' (Za~havi, 1975; Pomiankowski, 1988). If females are choosing mates based on traits which are signals of local adaptations (e.g. signals of good genes against parasites), genetic variation can be maintained due to the effects of co-evolution between parasites and hosts (Hamilton, 1982). The effects of sexual selection may act synergistically with decreased population size and restricted gene flow to increase the rates of divergence.

Schluter and Price (1993) presented a model which offers support for the role of sexual selection in the divergence of populations. Their model assumes direct benefits from mate choice, extendable to honest signals of good genes. If males present several traits signalling benefit, with varying degrees of detectability and honesty, females will exclusively prefer the single trait with the highest detectability × honesty value. This means that in two different habitats in which the detectability of two traits of equal honesty are reversed in rank, females will evolve to prefer different signals of benefit. Their model does not require genetic isolation between habitats and may allow sexual selection to act as a force interrupting gene flow, analogous to the effect of Fisherian sexual selection (Lande, 1982).

382 Mooers and MOller

The results presented here suggest that colonial breeding by itself may not facilitate higher levels of diversification. Only one of the three analyses supports the hypothesis. There may be several reasons for this, both biological and methodological.

Biologically, it may be that colonial species are not subject to significantly more intense sexual selection than socially monogamous birds. Perhaps their demographic structure does not facilitate speciation. In addition, we have little information on the rates of extinction among different groups of birds, as the fossil record is scanty (Feduccia, 1980). The results presented here assume that the extinction rates within colonial and non-colonial taxa are equivalent.

Methodologically, there are several issues. First, we must consider why the three analyses do not agree. The first test, which looked for an association between tribe size and the number of colonial species, may be viewed as exploratory. The correlations, while significant, were very low (Table 1). The test suffers the same problem as any comparative analysis which treats species values as independent data points (see Harvey and Purvis (1991) for a recent review of the problem). The sample size will be inflated if tribes with both many species and a high proportion of colonial species are close relatives (as occurs among shore and marine bird groups). A single change in the common ancestor of many present-day tribes to both colonial breeding and the ability to be species rich would then be counted many times. We need to look for independent co- occurrences of colonial lifestyle and species richness, as was attempted in the second and third analyses.

Regarding the third analysis, which used parsimony reconstructions, the tribe level designations were done using in-group comparison, which does not necessarily reconstruct the most parsimonious ancestral state. In addition, parsimony tends to be a poor model in situations where there are many changes in state, arguably the situation here. However, as most tribes contained a sizeable majority of either colonial or non-colonial species, there were few problematic tribe designations. Because only tribes where a majority of constituent genera are colonial are designated colonial, the method will tend to be conservative: no tribes designated colonial contain many non-colonial species. Still, it may be that for a few colonial tribes, the species counts are inflated because a few ancestrally non-colonial species are included. This would be a graver problem if an association between coloniality and diversity had been found based on the parsimony reconstructions, because any bias in the method would tend to inflate the size of colonial clades vis-dt-vis their non-colonial sister groups.

The final issue concerns the phylogeny used in the analysis. If it is wrong, then the tribes used may not be monophyletic and/or the sister group comparisons may be wrong. Sibley and Ahlquist's (1990) UPGMA tree has been strongly criticized (see Houde, 1987; Sarich et al., 1989); as with all comparative studies, the hypothesis concerning phylogenetic relationships is one of the assumptions underlying the results. While far from perfect, Sibley and Ahlquist's (1990) tree is the most extensive to date, has been corroborated in part by independent work (see Mooers and Cotgreave (1994) for a review), and has yielded novel ecological and evolutionary patterns (see, e.g. Cotgreave and Harvey, 1991, 1994; Nee et al., 1991, 1992; Saether, 1994).

Colonial breeding has almost certainly arisen independently a number of times during the evolution of birds (Siegel-Causey and Kharitonov, 1990). Patchiness of food resources away from the nesting sites (Horn, 1968; Lack, 1968), the type and abundance of predators (Hoogland and Sherman, 1976), the efficiency of information transfer among individuals (Brown, 1988; but see Shields, 1990), enticement to breeding areas by preferred males (MOller and Birkhead, 1993) and even entropy (Siegel-Causey and Kharitonov, 1990) have been given as possible causes for coloniality. Colonial breeding may have evolved for different reasons in different clades (Siegel- Causey and Kharitonov, 1990) and the differing regimes that selected for and now maintain colonial breeding might have opposing effects on speciation rates among clades.

Coloniality and speciation in birds 383

Coloniality alone does not seem to be a significant force generating diversity in the Aves. As the systematics of different well-studied clades become clearer, we will increasingly be able to test explicit hypotheses of correlates of diversity (see Nee et al., 1992). Barraclough et al. (1995) present data showing an association between sexual selection, measured as the proportion of species in a clade which are dimorphic, and diversity in Passerine birds, using the methods outlined in this paper. Our study and the work by Barraclough et al. (1995) highlight how birds offer an opportunity to study the broader question of the role of sexual selection in speciation. Studies comparing the potential and actual rates of evolution among species with different breeding systems would be welcome.

Acknowledgements

We thank Peter Cotgreave for access to his data on coloniality in non-passerine birds, Peter Cotgreave, Marion Petrie, Paul Harvey, John Marzluff, Dolph Schluter and several anonymous reviewers for comments on the manuscript and Tim Barraclough, Sean Nee, Marion Petrie and John Reynolds for discussion. A.O.M. was supported by a Natural Sciences and Engineering Council of Canada '1967' Scholarship and an Overseas Research Students Award (UK).

Data and references are available from the first author (e-mail: Mooers@zoology.ubc.ca).

References

Bakker, T.C.M. (1993) Positive genetic correlation between female preference and preferred male ornament in sticklebacks. Nature 363, 255-7.

Barraclough, T.G., Harvey, P.H. and Nee, S. (1995) Sexual selection and taxonomic diversity in passerine birds. Proc. R. Soc. B 259, 211-15.

Barrowclough, G.F. (1980) Gene flow, effective population sizes and genetic variance components in birds. Evolution 34, 784-98.

Bennett, P.M. (1986) Comparative studies of morphology, life history and ecology among birds. PhD thesis, University of Sussex.

Birkhead, T.R. and M¢ller, A.P. (1992) Sperm Competition in Birds: Evolutionary Causes and Consequences. Academic Press, London.

Brown, C.R. (1988) Enhanced foraging efficiency through information centers: a benefit of coloniality in cliff swallows. Ecology 69, 602-13.

Brown, C.R. and Brown, M.B. (1986) Ectoparasites as a cost of coloniality in cliff swallows (Riparia phyrrhonota). Ecology 67, 1206-18.

Bush, G.L., Case, S.M., Wilson, A.C. and Patton, J.L. (1977) Rapid speciation and chromosomal evolution in mammals. Proc. Natl Acad. Sci. USA 74, 3942-6.

Cotgreave, P. and Harvey, P.H. (1991) Bird community structure. Nature 353, 123. Cotgreave, P. and Harvey, P.H. (1994) Evenness of abundance in bird communities. J. Animal Ecol. 63,

365-74. Cracraft, J. (1984) Conceptual and methodological aspects of the study of evolution, with some comments

on bradytely in birds. In Living Fossils (N. Eldredge and S.M. Stanley, eds), pp. 95-104. Springer- Verlag, New York.

Dial, KP. and Marzluff, J.M. (1988) Are the smallest organisms the most diverse? Ecology 69, 1620-4. Farrell, B.D., Dussourd, D.E. and Mitter, C. (1991) Escalation of plant defense: do latex and resin canals

spur plant diversification? Am. Nat. 138, 881-900. Farris, J.S. (1976) Expected asymmetry of phylogenetic trees. Syst. Zool. 25, 196-8. Feduccia, A. (1980) The Age of Birds. Harvard University Press, Cambridge, MA. Felsenstein, J. (1985) Phylogenies and the comparative method. Am. Nat. 125, 1-15. Fisher, R.A. (1930) The Genetical Theory of Natural Selection. Oxford University Press, Oxford. Fisher, R.A. and Yates, F. (1975) Statistical Tables for Biological, Agricultural and Medical Research.

Longman, London.

384 Mooers and M¢ller

Fitch, W.M. (1971) Towards defining the course of evolution: minimal change for a specific tree topology. Syst. ZooL 20, 206-16.

Guyer, G. and Slowinski, J.B. (1993) Adaptive radiation and the topology of large phylogenies. Evolution 47, 253-63.

Hamilton, W.D. (1982) Pathogens as causes of genetic diversity in their host populations. In Population Biology of Infectious Diseases (R.M. Anderson and R.M. May, eds), pp. 269-98. Springer-Verlag, Berlin.

Harvey, P.H. and Mace, G.M. (1982) Comparisons between taxa and adaptive trends: problems of methodology. In Current Problems in Sociobiology (Kings College Sociobiology Group, eds), pp. 343-61. Cambridge University Press, Cambridge.

Harvey, P.H. and Purvis, A. (1991) Comparative methods for explaining adaptations. Nature 351, 619-24.

Heard, S.B. and Hauser, D.L. (1995) Key evolutionary innovations and their ecological mechanisms. Hist. Biol. 10, 151-73.

Hoogland, J.L. and Sherman, P.W. (1976) Advantages and disadvantages of bank swallow (Riparia riparia) coloniality. Ecol. Monogr. 46, 33-58.

Horn, H.S. (1968) The adaptive significance of colonial nesting in the Brewer's blackbird (Euphagus cyanocephalus). Ecology 49, 682-94.

Houde, P. (1987) Critical evaluation of DNA hybridization studies in avian systematics. Auk 104, 17-32. Kochmer, J.P. and Wagner, R.H. (1988) Why are there so many kinds of passerine birds? Because they are

small: a reply to Raikow. Syst. Zool. 37, 68-9. Lack, D. (1968) Ecological Adaptations for Breeding in Birds. Methuen, London. Lande, R. (1982) Rapid origin of sexual isolation and character divergence in a cline. Evolution 36,

213-23. Launder, G.V. (1981) Form and function: structural analysis in evolutionary morphology. Paleobiology 7,

430-42. Marzluff, J.M. and Dial, K.P. (1991) Does social organization influence diversification. Am. Midl. Nat. 125,

126-34. May, R.M. (1986) The search for patterns in the balance of nature: advances and retreats. Ecology 67,

1115-26. M¢ller, A.P. and Birkhead, T.R. (1992) A pairwise comparative method as illustrated by copulation

frequency in birds. Am. Nat. 139, 1089-101. M¢ller, A.P. and Birkhead, T.R. (1993) Cuckoldry and sociality: a comparative study of birds. Am. Nat.

142, 118-40. Mooers, A.~. and Cotgreave, P. (1994) Sibley and Ahlquist's tapestry dusted off. Trends Ecol. Evol. 9,

458-9. Morton, E.S., Forman, L. and Braun, M. (1990) Extrapair fertilizations and the evolution of colonial

breeding in purple martins. Auk 107, 275-83. Nee, S., Read, A.F., Greenwood, J.J.D. and Harvey, P.H. (1991) Phylogeny and the relationship between

abundance and body size in British birds. Nature 351, 312-13. Nee, S., Mooers, AD. and Harvey, P.H. (1992) Tempo and mode of evolution revealed from molecular

phylogenies. Proc. Natl Acad. Sci. USA 89, 8322-6. Nee, S., Barraclough, T.G. and Harvey, P.H. (in press) Temporal changes in biodiversity: detecting patterns

and identifying causes. In Biodiversity: A Biology of Numbers (K.J. Gaston, ed.). Oxford University Press, Oxford.

Pagel, M.D. (1992) A method for the analysis of comparative data. J. Theor. Biol. 156, 431-42. Pagel, M.D. (1993) Seeking the evolutionary regression coefficient: an analysis of what comparative

methods measure. J. Theor. Biol. 164, 191-205. Pomiankowski, A.N. (1988) The evolution of female mate preferences for male genetic quality. Oxf Surv.

Evol. Biol. 5, 136-84. Purvis, A. and Rambant, A. (1995) Comparative analysis by independent contrasts (CAIC): an Apple

Macintosh application for analysing comparative data. CABIOS 11, 297-51.

Coloniality and speciation in birds 385

Saether, B.-E. (1994) Reproductive strategies in relation to prey size in altricial birds: homage to Charles Elton. Am. Nat. 144, 285-99.

Sarich, V.M., Schmid, C.W. and Marks, J. (1989) DNA hybridization as a guide to phylogenies: a critical analysis. Cladistics 5, 3-32.

Schluter, D. and Price, T. (1993) Honesty, perception and population divergence in sexually selected traits. Proc. R. Soc. B 253, 117-22.

Shields, W.M. (1990) Information centers and coloniality in cliff swallows: statistical design and analysis - a comment. Ecology 71, 401-5.

Sibley, C.G. and Ahlquist, J.E. (1990) Phylogeny and Classification of Birds: A Study of Molecular Evolution. Yale University Press, New Haven, CT.

Sibley, C.G. and Monroe, B.L. (1990) Distribution and Taxonomy of the Birds of the World. Yale University Press, New Haven.

Siegel-Causey, D. and Kharitonov, S.P. (1990) The evolution of coloniality. Curr. Ornithol. 7, 285-330. Slowinski, J.B. (1990) Probabilities of n-trees under two models: a demonstration that asymmetrical inferior

nodes are not improbable. Syst. Zool. 39, 89-94. Slowinstd, J. and Guyer, C. (1994) Testing whether certain traits have caused amplified diversification: an

improved method based on a model of random speciation and extinction. Am. Nat. 142, 1019-24. Sokal, R.R. and Michener, C.D. (1958) A statistical method for evaluating systematic relationships. Univ.

Kansas Sci. Bull 38, 1409-38. Sokal, R.R. and Rohlf, F.J. (1981) Biometry. W.H. Freeman, New York. Stanley, S.M. (1979) Macroevolution: Pattern and Process. W.H. Freeman, San Francisco, CA. Swofford, D.L. and Maddison, W.P. (1987) Reconstructing ancestral character states under Wagner

parsimony. Math Biosci. 87, 199-229. Swofford, D.L. and Olsen, G.J. (1990) Phylogeny reconstruction. In Molecular Systematics (D.M. Hillis and

C.J. Moritz, eds), pp. 411-501. Sinauer Associates, Sunderland, MA. Van Valen, L. (1973) Body size and numbers of plants and animals. Evolution 27, 27-35. Wagner,, R.H. (1993) The pursuit of extra-pair copulations by female birds: a new hypothesis of colony

formation. J. Theor. Biol. 163, 333-46. Wilson, E.O. (1975) Sociobiology. Belknap Press, Cambridge, MA. Wittenberger, J.F. and Hunt, G.L. (1985) The adaptive significance of coloniality in birds. Avian Biol. 8,

882-91. Wright, S. (1978) Evolution and Genetics of Populations. University of Chicago Press, Chicago, IL. Zahavi, A. (1975) Mate selection - a selection for a handicap. J. Theor. Biol. 53, 205-14.