Clade extinction appears to balance species diversification in sister lineages of Afro-Oriental passerine birds

Transcription

1 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 1 Clade extinction appears to balance species diversification in sister lineages of Afro-Oriental passerine birds Robert E. Ricklefs and Knud A. Jønsson Supplementary Information, Appendices S1-S16 Appendix S1. The regional setting. The total area of the Afrotropic region (ca km 2 ) exceeds that of the Oriental region (ca km 2 ) by a factor of more than 3, but the area of tropical and subtropical moist broadleaf forest, which supports a large part of the passeriform diversity in each of the regions, favors the Oriental region (5.40 versus km 2 ) (1, ) (Fig. S1). India was geographically integrated into the Oriental region by 50 Ma, leaving open ocean with scattered small islands to support dispersal across the Indian Ocean between the two biogeographic regions (2, 3). Land areas north and south of the early Tertiary Tethys Sea, including the Arabian Peninsula underwent uplift around 35 Mya (4), potentially facilitating early movement of birds between the regions, although the Tethyean region also cooled and became more arid after this time until the onset of a more mesic period 20 Mya (5). During the Miocene Epoch, the climate of the Arabian Peninsula was cooler and more mesic than earlier during the Oligocene, and wetter than at present. Many species of mammal crossed between the regions at this time and dispersal routes were undoubtedly available for many types of birds (6-8). Fig. S1. Map of present-day ecoregions from (1). Dark green areas are tropical and subtropical moist broadleaf forests. Light green areas represent various types of dry forests, shrublands, grasslands, and savannas. Cream coloured areas are deserts and arid regions. The inset map shows the areas of the African (red) and Oriental (dark blue) regions included in this study.

2 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 2 Appendix S2. Influence of taxonomy. Using an older taxonomic concept (IOC World Bird Names list version 1.0) (9), the logarithms of the number of species in each of 29 shared families, which totaled 1006 species in Africa and 840 species in southern Asia, were positively correlated (Pearson r = 0.37, P = 0.052; Spearman r = 0.43, P = 0.02). Using a newer taxonomy (IOC World Bird Names list v 3.3) (10) (35 shared families, 944 species in Africa and 666 species in southern Asia), the correlation was not correlated (Pearson r = 0.25, P = 0.15; Spearman r = 0.29, P = 0.09). Although the numbers of species per family are not correlated between African and the Oriental biogeographic realms, these analyses do not necessarily involve sister group comparisons, as the species in one region might be paraphyletic, or multiply paraphyletic, with respect to the other region. For this reason, we focus on the descendants of nodes separating sister clades in the two regions. Appendix S3. Clade sizes are not correlated between regions. The log-transformed sizes of AF and OR clades of passerine birds are positively correlated (r = 0.55, p < , n = 150), but part of this is related to the effect of clade age on number of species, and also to a concentration of nodes having one species in both regions (many are young colonists; this is the initial condition). The residuals from the ln(species) vs. age regressions in each region are also correlated (r = 0.24, p = ), suggesting that there might be some correlation in diversification rates (i.e., an inheritance of diversification rate), but the correlation is low (R 2 < 0.05). The significant correlation between the residuals for the two regions appears to be driven by a concentration of positively related residuals near the center of the plot (Fig. S2). The correlation for nodes > 5 Ma is r = (p = 0.33, n = 98); the correlation for nodes for which both AF and OR > 1 species is r = (p = 0.41; n = 86). This restriction eliminates the line of clades with equal deviations, i.e., the diagonal in the graph (black symbols in Fig. S2). Residuals of the number of species in sister clades of non-passerine birds from the regressions of the logarithm of species as a function of age for the AF and OR clades also were not significantly correlated (r = 0.16, p = 0.20). Fig. S2. Residuals from the regression of the natural log of clade size versus clade age for sister clades in the Afrotropical and Oriental biogeographic regions. The correlation is not significant when nodes represented by clades of one species in both regions (solid symbols) are left out of the calculation. Residuals for Oriental clades (ln species) 4 single species in both regions n = 86, r = 0.09, p = Residuals for African clades (ln species)

3 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 3 Appendix S4. The influence of region of origin on clade size. The relative sizes of sister clades that have diversified in different regions might differ in one direction or the other, depending on underlying influences. On one hand, a clade might diversify more readily in the region of origin than in a new area because of its prior history of diversification there and adaptation to local conditions. On the other hand, a newly colonized area would lack closely related competitors and therefore present open ecological space for the new lineage (11). We attempted to infer the area of origin of the lineages derived from each node in our phylogeny by (a) the topology of nestedness of the clades (Appendix S16, Fig. S7) and (b) ancestral area analysis using maximum likelihood as implemented in the R (R Development Core Team 2013) package APE (Paradis et al. 2004). The ancestral locations of almost one-third of the nodes (49 of 150) could not be assigned unambiguously on the basis of topology. The sizes of clades with ambiguous origins were larger than those with origins assigned to either region, primarily because these represented older nodes (14.4 Ma versus 8.3 [AF] and 9.7 [OR] Ma). The number of species in sister clades with both African origins and Oriental origins were greater in the region of origin than in the newly colonized region (Fig. S3); in the Oriental region, the sizes of clades with Oriental origins exceeded the sizes of clades with African origins. Natural logarithm of average clade size Origin in Africa Origin in the Orient Origin ambiguous Clade size in Africa Clade size in the Orient Fig. S3. Log-transformed number of species in clades of African and Oriental origin in Africa and the Orient. In Africa, clades with different origins did not differ in size (t = 0.94, p = 0.35), whereas in the Oriental region, clades that originated in the Orient were larger than those that originated in Africa (t = -2.24, p = 0.029; Satterthwaite correction for unequal variance). In Africa, after removing the effect of age on clade size, neither the region of origin nor the region-times-age interaction was significant (p > 0.05); in the Orient, the increase in species with age of clade exhibited a significant interaction between age and region of origin, with rate of exponential increase equal to for Oriental clades and for African clades (t = -3.2, p = 0.002). We repeated the previous analysis with an Oriental origin assigned to nodes with posterior probabilities of occurring in the Orient greater than 0.60; nodes were assigned African origins if the posterior probability of occurring originally in the Orient was less than More than half the clades (84) had ambiguous origins with these criteria, leaving 37 with inferred African origins and 29 with inferred Oriental origins. The mean ages of the assigned African nodes (14.61 ± 8.95 SD Ma) and Oriental nodes (16.00 ± 9.59 SD Ma) exceeded the ages of the ambiguous nodes (7.02 ± 6.90 SD Ma), which was the reverse of topologically assigned node origins. As in the case of using topologically assigned node origins, descendant clades were

4 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 4 larger (log-transformed number of species) in the region of origin than in the region of introduction (AF origins: 1.74 ± 1.25 SD versus 0.98 ± 1.38 sd; OR origins: 1.85 ± 0.98 SD versus 1.24 ± 1.20 SD). Although clades from both regions were larger in the area of origin than in the area introduction, the differences between clade sizes within each region were only marginally significant in Africa (AF: t = 1.67, P = 0.10; OR: t = 2.9, P = 0.005). When clade age was included in this analysis, the age*origin interaction term was marginally significant in both AF (t = 1.91, P = 0.060) and OR (t = 2.04, P = 0.046). The discrepancy between these two analyses reflects the fact that clades with OR origins were somewhat older, on average (16.0 ± 9.60 SD Ma) than clades with AF origins (14.6 ± 8.95 SD Ma). Appendix S5. Species-age relationship. We used a series of general linear regression models (SAS Procedure GLM) for the relationship between clade size and clade age to test whether the intercept differed significantly from 0, whether the relationship deviated from linearity (tested by the significance of a quadratic term), and whether weighting each node by its posterior probability had any effect on the quality of the regression. In all cases, intercepts did not differ from 0 (P > 0.05). The R 2 values for the intercept regressions (AF: R 2 = 0.428; OR: R 2 = 0.404) were not increased significantly by the weighting factor (R 2 = and 0.372, respectively), and so weights were not included. In both intercept regressions and regressions through the origin, quadratic terms did not improve the fit (P > 0.05), and so the final models were linear regressions passed through the origin: for the African clades, b = ( SE), F = 250 (1,149 df), P < , R 2 = 0.626; for the Oriental clades, b = ( SE), F = 218 (1,149 df), P < , R 2 = We also used nonlinear regression to fit the relationship between number of species (N) and age (t) when the extinction rate is a certain proportion ( ) of the speciation rate ( ), ( ) ( ( ) ) ( ) (Equation S1) (12-14). For the clades in both the Oriental and African regions, was estimated to be 0, in which case the equation S1 reduces to ln(n) = ln(exp[ t]), which is the log-linear relationship lnn = t evaluated above. Appendix S6. Increase in variation in species number with clade age. In a random speciation extinction process, the expected variance in the size of extant clades is N(N - 1), or approximately the square of clade size, where N is the average number of species per clade. Hence, the log of the variance should increase at twice the exponential rate as the average number of species, and the log of the standard deviation should increase at the same exponential rate as the number of species. Although one cannot calculate the variance in number of species in clades of different ages, the absolute values of the deviations also should increase at nearly the same exponential rate as the mean number of species. The latter prediction is fairly well met in regressions of the absolute residuals of the logarithms of clade size for the African clades: b = ( SE); and for the Oriental clades: b = ( SE). As explained in the previous paragraph, the rates of increase in the logarithms of clade size with age were and 0.075, respectively. Another approach to the increase in variance with time is to estimate an exponential rate of increase in the size of clades (N) over time (t), and then to estimate the exponential rate of increase in the residuals (N i N predicted ) over time. In a random process, these should increase at the same rate. These estimates were produced using the SAS Procedure NLIN to fit a simple exponential function, N i = exp(bt). With respect to the number of species per clade (N i > 0), the

5 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 5 estimate for AF was b = ( SE) Ma -1 (95% CI = ) (R 2 = 0.39); for OR, the estimate was b = ( SE) Ma -1 (CI: ) (R 2 = 0.12). The absolute values of the residuals were also related to age with the following results: AF, b = ( SE) Ma -1 (CI = ) (R 2 = 0.710); OR, b = ( SE) (CI = ) Ma -1 (R 2 = 0.154). The 95% confidence limits of these values include the rate of increase in clade size itself. Note also that the AF regressions have much higher R 2 values than the OR regressions in this comparison. Appendix S7. Diversification of non-passerine clades in the Oriental and African regions. Terrestrial environments in tropical Africa and southern Asia are inhabited by many orders of small non-passerine birds including woodpeckers (Piciformes), doves (Columbiformes), and cuckoos (Cuculiformes), among others (Trogoniformes, Coraciiformes, Apodiformes, and Caprimulgiformes). Many of these orders are very old, and they may have been replaced ecologically to a large extent by the diversification of passeriform birds during the past 40 Ma (15, 16). Accordingly, we performed a parallel analysis on these orders of non-passerine species to compare patterns of diversification. If the non-passerine orders have been replaced by the Passeriformes, we could expect to see a reduced rate of diversification and evidence of slowdown in diversification toward the present. The 68 clades identified in the 7 orders included 277 species-level taxa in Africa and 216 in the Oriental region. Of the 68 nodes, 52 were terminal; only 19 of the nodes had support values exceeding 95%, with an additional 12 having support values exceeding 50%; average node age was 16.7 ± 11.2 SD Ma, which is considerably older than the average node age for the passerines (10.6 ± 8.9 SD Ma, P < 0.001). Regressions of the logarithm of clade size versus age revealed no departures from linearity (quadratic terms insignificant) and no significant differences of the intercepts from the origin (lnn = 0) in linear models. Thus, the data do not suggest a departure from time-homogeneous exponential growth dominated by speciation, as we also found for passerine clades. Linear regressions of the logarithm of clade size as a function of time fitted through the origin had slopes of ( SE) for the African clades and ( SE) for the Oriental clades. These slopes are lower than for the passerine clades (0.063 and 0.075, respectively). The accumulation of nodes back in time can be fitted by an exponential approach to an asymptote (see main manuscript, Fig. 3) with the colonization rate C = 3.00 (0.12 SE) and the extinction rate E = ( SE). Accordingly, the asymptotic number of clades would be C/E = 3.00/0.032, or close to 100 (compared to the 68 clades in the analysis). As pointed out above, when clades diversify by a random birth-death process that is homogeneous across clades, the variance in number of species increases in proportion to the square of the mean and the standard deviation increases in proportion to the mean. Since the mean increases exponentially at rate r, the standard deviation should increase exponentially at the same rate. We calculated absolute deviations of clade sizes for non-passerine birds from the exponential fit of clade size to age, and then used a non-linear regression to fit these absolute residuals as a function of time with an exponential function. The exponential rates of increase in number of species were AF = ( SE) and OR = ( SE). These slopes are a little higher than those for the linear regressions on the log-transformed variables (0.52 and 0.36, respectively). The exponential rates of increase in the absolute residuals from the above exponential regressions were ( SE) for Africa and ( SE) for the Orient, which match well the expectation of an exponential increase. Thus, the overall rate of increase in

6 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 6 the nonpasserine clades is somewhat less than for the passerines, but they seem to be undergoing similar diversification processes. Note, in both cases, that the agreement between the rate of increase in number of species and the residuals from the exponential regressions indicates that the rate of diversification is homogeneous across clades. If each clade had a different rate of diversification, the increase in the residuals would exceed the rate of increase in number of species with time. Appendix S8. Likelihood analysis of the species-age relationship. The likelihood of obtaining n species after time t with random speciation at rate b and random extinction at rate d is ( ) ( ) [ ( ) [ ( ), where ( ) ( ) (13, 14). Log-likelihoods were calculated for each combination of b and d from b = 0.01 to 0.31 Ma -1 by increments of 0.01 Ma -1, and d = 0.00 to b by 0.01 Ma -1. The maximum likelihood model for the 150 Oriental clades was b = 0.12 and d = 0.00 Ma -1, and for models with lnl < 4, (b d) varied between 0.09 and 0.12; for the 150 African clades, the maximum likelihood model was b = 0.17 and d = 0.07, and for models with lnl < 4, (b d) varied between 0.07 and These estimates are consistent with both the linear and nonlinear models discussed in Appendix S5. Appendix S9. Comparison of exponential and logistic models of clade growth. An appropriate model for diversity-dependent limitation of the diversification rate within a clade is the logistic model, in which rate of diversification decreases linearly with increase in clade size (17). The logistic model can be written as ( ) where A is the asymptote, or upper limit, for the number of species, k is the exponential rate of clade growth without diversity limitation (i.e., at low clade size) and t i is the time at which the inflection point of the growth curve is reached, i.e., when growth shifts from accelerating to decelerating, achieved at A/2 in the case of logistic growth. We compared exponential and logistic models of growth by F-tests based on ratios of the error mean squares (see Table S1). For both the African and Oriental clades, the error sums of squares (ESS) for the logistic models were >90% of the ESS values for the exponential model (F < 1.10, P > 0.50, df = 148, 146). Thus, we have no statistical basis for preferring a constrained, logistic model over an unconstrained, exponential model of clade growth. In addition, only 12 of the African clades and 13 of the Oriental clades (out of 150 in each region) exceeded A/2 species and would be in the decelerating phase of logistic clade growth.

7 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 7 Table S1. Parameters of logistic equations fitted to the relationship of clade size and age in the African and Oriental regions (standard errors in parentheses). Parameter (units) Africa Orient A (species) (13.78) (8.17) K (Ma -1 ) (0.053) (0.046) t 50 (Ma) 24.6 (5.1) 22.9 (7.1) Error MS (df = 146) Appendix S10. Analysis of nodes with 50% and 80% posterior support. We conducted analyses identical to those applied to the full dataset but restricted to nodes uniting Oriental and African clades having 50% posterior probabilities (PP) (n = 53) or 80% posterior probabilities (n = 43). The results are summarized in Table S2. Number of species per clade in Africa, but not the Orient, increase with increasing node posterior probability because many of the smaller clades in Africa derive from poorly supported nodes. However, the exponential rates of increase in number of species with age of clade vary little across the samples and remain consistent with a time- and clade-homogeneous process of diversification with little evidence of extinction. The rate of colonization (node statistic C) is lower for the reduced datasets because fewer nodes are included and also because the shape of the node accumulation curve is flatter, resulting in lower values of both the rate of node extinction (E) and the estimated asymptotic number of nodes (C/E). The extinction rate in the more strongly supported nodes is also lower because the descendant clades of many of the nodes with weak support had few species. Table S2. Statistics for nodes and clades based on samples of nodes with levels of posterior support greater than 0, 50%, and 80%. Standard deviations are reported for number of species and ages of nodes; standard errors are reported for estimated parameters. Variable Region PP > 0 (n = 150) PP > 0.50 (n = 53) PP > 0.80 (n = 43) Number of species AF 7.6 ± 21.2 (1-205) 12.8 ± 33.1 (1-205) 14.6 ± 36.5 (1-205) OR 6.2 ± 23.5 (1-274) 6.1 ± 9.8 (1-58) 6.6 ± 10.6 (1-58) Age of nodes Nodes 18.5 ± 11.1 (0-40) 15.7 ±10.1 (1-39) 16.0 ± 10.7 (1-39) C Nodes 12.6 ± ± ± 0.08 E Nodes ± ± ± C/E Nodes Ln(N) = b*age AF ± ± ± (value of b) OR ± ± ± N = exp(b*age) AF ± ± ± (value of b) OR ± ± ± SD of residuals of exponential fit AF ± ± ± OR ± ± ± 0.005

8 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 8 Appendix S11. IUCN status of single-species clades. One index to the vulnerability of a species to extinction is its IUCN Red List status ( Based on assessments of population sizes and trends, and potential threats to species survival, the IUCN ranks species risk of extinction from Least Concern (LC), to Near Threatened (NT), Vulnerable (VU), Endangered (EN), Critically Endangered (CR), Extinct in the Wild (EW), and Extinct (EX). We tabulated these assessments for single-species clades in the Oriental (60 species) and African (31 species) biogeographic regions, and compared them with a random selection of species regardless of clade size (53 AF and 38 OR species) (Table S3). Similar numbers of species were in the group Least Concern (72 and 74 species) and the groups Near Threatened and Vulnerable (14 and 13 species). Thus, single-species clades do not appear to be closer to the brink of extinction than species selected at random from larger clades. Table S3. Distribution among IUCN Red List categories of species in single species clades in the African and Oriental biogeographic regions and a random selection of species regardless of clade size and region. IUCN Red List category Singlespecies clades Randomlyselected species Least concern Near threatened 7 9 Vulnerable 7 4 Endangered 1 0 Critically endangered 2 1 Not available 1 3 Data deficient 1 0 Total Appendix S12. Clade increase under constant speciation and extinction. Under a timehomogeneous process, the average size of extant clades increases as ( ) ( ) and the probability that a new clade survives to age t is ( ) ( ) ( ), (Equation S2) ( ), (Equation S3) where and are the speciation and extinction rates, respectively (18). As t becomes large, N(t N > 0) approaches an exponential increase in species richness according to e ( - )t /( ), and P(N > 0 t) approaches a constant level of 1 /. Although N(t N > 0) approaches a constant exponential rate regardless of the rate of extinction, the relationship between N and t is nonlinear at low t and linear regressions of logn as a function of t have significant intercepts at N(t = 0) > 1. Representative outcomes of these processes are shown in Fig. S4. In the extreme case, when the species extinction rate ( ) equals the speciation rate ( ), the probability that a newly formed clade (N = 1) is extinct at time t is P(N = 0 t) = t/( t + 1) (19). In addition, the expected size of extant clades at time t is t + 1, i.e., average clade size increases approximately linearly with time, rather than exponentially. Under a balanced speciation-extinction process ( = ), the probability of extinction of a newly formed clade (N 0 =

9 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 9 1) over one time unit is /( + 1). Thus, for a node survival rate (1 E) of 0.92 Ma -1, and the inferred clade extinction rate of 0.5E = 0.04 Ma -1, which we estimated from the cumulative increase in number of nodes with age (Main text Fig. 3), /( + 1) = 0.04, and = = However, although this value matches the observed clade survival rate inferred from the node survival rate, it cannot generate the clade sizes observed in this analysis, and it predicts close to a linear rate of increase in clade size over time rather than the observed exponential rate of increase (Main text Fig. 4). Number of species per clade Age of clade (Ma) Age of clade (Ma) Fig. S4. Expected mean number of species per extant clade (left panel) and proportion of surviving clades (right panel) as a function of clade age, both plotted on logarithmic scales, under different combinations of speciation and extinction rates (legend in left-hand panel) ranging from an extinction rate of 0 ( = 0.09, = 0.0) to ca. 97.5% of the speciation rate ( = 0.41, = 0.40). The clade extinction rate decreases with age as the average size of clades increases. Appendix S13. Model fits and simulated clade statistics. Main text Fig. 4 shows the results of simulations of a random speciation-extinction process with three combinations of rates and begun with sufficient lineages to result in approximately 150 extant clades after 40 Ma of simulation ( Ma time steps). Statistics for the simulated data in each of the panels are as follows: Panel A: = 0.09 Ma -1, = 0.00 Ma -1 ; 150 nodes at the beginning and end of the simulation (ages ± SD Ma); species per clade, region 1 (closed symbols), 6.27 ± 6.30 (1-72), region 2, 7.88 ± 7.93 (1-90); linear regressions of the logarithms of the simulated clade sizes with respect to time, passed through the origin, had slopes of ( SE) and ( SE) Ma -1. Note that these slopes are about one-quarter less than the rate of speciation used in the simulation. Nonlinear exponential regressions yielded slopes of (SE = 0.002, 95% CI = ) and (SE = 0.002, 95% CI = ), hence very close to the input speciation parameter. Panel B: = 0.16 Ma -1, = 0.10 Ma -1 ; 149 nodes (ages ± SD Ma) remaining from an initial 500 nodes; species, region 1, 6.00 ± 8.68 (1-68), region 2, 7.28 ± (1-84). The node accumulation (inset) is fit by C = 9.80 ± 0.21 SE Ma -1, E = ± SE Ma -1. The slopes of the linear regressions passing through the origin are ( SE) and ( SE) Ma -1, which are similar to the empirical values for African and Oriental clades, and Proportion of clades remaining

10 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 10 about 30% higher than the net diversification rate ( = 0.06) employed in the simulation. Panel C: = 0.41 Ma -1, = 0.40 Ma -1 ; 153 nodes (ages 5.57 ± 8.05 SD Ma) remaining from an initial 2500 nodes; species, region 1, 3.40 ± 6.27 SD (1-44), region 2, 3.74 ± 6.94 SD (1-61). Node accumulation rate, C = ± 0.62 SE Ma -1, E = ± SE Ma -1 ). The increase in clade size with time was best fit by a quadratic relationship passed through the origin (linear terms ± SE and ± SE; quadratic terms ± SE and ± SE; coefficients of determination, 0.57 and 0.74, respectively). The last simulation (Panel C) approximated clade diversification under a balanced speciation-extinction process that generated an appropriate range of clade sizes. Rates of node formation (C) and extinction (E) were high because most of the young clades with small numbers of species went extinct quickly. Clade sizes resembled those observed in the African and Oriental clades, but the linear relationship between lnn and clade age had a significant positive intercept, and the clade accumulation curve suggested a rate of node initiation four times that estimated from the observed data. Statistics for these and additional simulations, including the clade extinction model and clade origination model, are presented in Table S4. Table S4. Characteristics of simulated clades produced under different rates of speciation ( ) and extinction ( ) compared to those of observed clades. Simulated clades Singletons SD/Mean Estimated node formation and extinction Clade age Clades Africa Orient Area 1 Area 2 C E Mean SD (0.62) (0.0059) (0.43) (0.0041) (0.38) (0.0037) (0.21) (0.0024) (0.05) (0.0009) Clade extinction model* (0.13) (0.0013) Clade origination model (0.06) (0.0007) Observed (0.07) (0.0008) Note: *In the clade extinction model, clades suffer extinction at a rate of 0.07 per Ma regardless of their size or age. In the clade origination model, the probability of clade origination decreases exponentially towards the past at an exponential rate of , i.e., from 1 at 0 Ma (the present) to 0.22 at 20 Ma and 0.05 at 40 Ma. Results of the simulation with = 0.41 and = 0.40 are presented in the main text Fig. 4, Panel C; = 0.16 and = 0.10, Fig. 4, Panel B; = 0.09 and = 0.00, Fig. 4, Panel A.

11 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 11 Appendix 14. Nonrandom selection of taxonomically distinguished clades. An issue with many previous studies has been that clades were chosen for analysis nonrandomly. In particular, clades may be selected from studies of time-calibrated phylogenetic relationships of species within named taxa, often genera or families, of a convenient size typically not too small to be uninteresting. As a result, clades of small size are absent from these analyses, which gives the appearance of clade size being independent of clade age. For example, Fig. S5 shows data for avian clades analyzed by Phillimore and Price (20), none of which include fewer than 8 species, and, for comparison, the clades treated in this analysis. The failure to include small clades biases the slope of the species-versus-clade-age relationship downward, and gives the appearance of a slowing of the rate of diversification or, alternatively, a nearly balanced speciation-extinction process with a relatively high extinction rate. This figure also compares our analysis to that of McPeek et al. (21), who related clade size to age in multiple monophyletic groups of birds. In their analysis, the slope of the relationship was zero, suggesting that clade diversity is constrained within limits regardless of age. Number of species African clades Oriental clades Phillimore and Price (2008) McPeek (2008) Age of clade (Ma) Fig. S5. Comparison of the relationships between clade size and clade age (solid lines) portrayed by Phillimore and Price (2008) and McPeek (2008) and the relationship obtained in the present study (dashed lines). Appendix S15. Interpretation of lineage-through-time (LTT) plots. LTT plots represent the branching times of the directly ancestral lineages of modern taxa, and they are shaped by a number of processes in addition to the history of diversification. When there is no extinction in the history of a clade, the LTT plot provides an unbiased estimate of the rate of speciation through time. If both speciation and extinction are time-homogeneous, the LTT plot provides an unbiased estimate of the rates of these processes (18, 22, 23). However, apparent declines in the rate of diversification also can be produced by failure to recognize incipient speciation events, which would tend to produce a leveling of the LTT plot close to the present, essentially over the period required for the formation of lineages that are sufficiently differentiated to be recognized

12 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 12 as different species. Another cause of a leveling of the LTT plot deeper in a clade would be the initiation of a clade extinction phase, whereby contemporary species and their immediately ancestral lineages are trimmed from the phylogeny. Because ancestral lineages closer to the origin of a clade have more descendants, on average, they are less likely to be trimmed by recent extinctions, which will give the appearance of a leveling off of the LTT plot towards the present. We expect such patterns from the clade extinction model put forward in this paper. LTT plots for eight of the largest clades from Africa and the Orient (Figure S6) illustrate typical patterns. The LTT plot for clade 2631OR (dark red) is close to linear (left panel) and the number of nodes in each time period increases exponentially (right panel), as one expects from a time homogeneous process dominated by speciation. Clades 2105AF (black) and 2715OR (blue) exhibit reasonably linear LTT plots until the last time interval, when the number of nodes drops dramatically below the exponential expectation. Potential causes of this pattern include failure to recognize incipient species (which might be a clade-specific property) or the recent inception of a clade extinction process. Other clades that exhibit a gradual leveling off of the LTT plot (e.g., 3285AF [pink], 2459OR [cyan], 2715AF [red]), could represent either diversity-dependent decline in diversification rate or clade extinction events. Without additional information unavailable to us (e.g., from the fossil record), these possibilities cannot be distinguished. Number of lineages Lineage through time plots Time from clade origin (Ma) 2105AF 2459OR 2715AF 2715OR 2631OR 3059AF 3258AF 3608AF Number of nodes per 3 Ma interval AF 2459OR 2715AF 2715OR 2631OR 3059OR 3258AF 3608AF 25 Nodes through time plot Millions of years before present 5 0 Fig. S6. Lineage-through-time (LTT) plots (left panel) and node density through time (NTT) plots (right panel) for eight of the largest African and Oriental clades included in our dataset. Node densities are the number of nodes in a phylogeny in successive 3-Ma time intervals. A time-homogeneous pure speciation process produces log-linear LTT and NTT plots. As time-homogeneous extinction is added to the process, the initial rise in the LTT plot becomes steeper, as shown by several of the clades (e.g., 3608AF and 3258AF). A phase of recent extinction will produce a leveling off of the LTT plot and a decline in the number of nodes per interval (e.g., 3258AF, 2715AF). Appendix S16. Designation of sister clades. We identified sister relationships in the phylogenies for passerine and nonpasserine birds using the following criteria (Fig. S7): node rank 1, a terminal split between clades occurring uniquely in OR and AF, that is (OR*AF), where * indicates the node in question; node ranks 2-4, subterminal nodes were included only if the descending branches clearly belonged to different regions. Thus (AF*(AF,OR)) is ambiguous because both branches could be AF. In contrast, we included (AF*(OR,(AF,OR))) and ((AF,(AF,OR))*(OR,(AF,OR))) because one infers that the basal branches are in different

13 Ricklefs and Jønsson, diversification of Afro-Oriental passerine birds, SI Appendices, page 13 regions. In contrast, ((AF,OR)*(OR,(AF,OR))) was not included because both basal branches could be OR. The passerine phylogeny included 150 nodes separating Oriental and African clades, 105 of which were terminal (rank 1); the remainder were subterminal (rank 2 = 30; rank 3 = 12; rank 4 = 3). The nonpasserine phylogeny included 68 nodes, 52 of which were terminal (rank 1). We inferred the region of origin of each pair of sister clades when the node joining the clades was clearly nested within ancestral clades restricted to one or the other region. We also used the ACE function of the package APE (24) in R version (R Development Core Team 2013) to reconstruct ancestral areas using maximum likelihood (ML) for each node in the phylogeny. The correspondence between topological and maximum likelihood estimates of ancestral areas was poor. For example, ML probabilities for an Oriental origin were 0.56 ± 0.17 SD for nodes judged to be Oriental topologically, 0.47 ± 0.19 SD for nodes judged to be African in origin, and 0.44 ± 0.19 SD for nodes that were ambiguous (F = 5.2, df = 2, 147, P = ). Fig. S7. Topological identification of dispersal events with sister clades in each region, and inference of the ancestral area and direction of dispersal based on paraphyly (clade nestedness). Two node comparisons are illustrated in the diagram (brackets), one nested within the other. Literature Cited 1. Olson DM, et al. (2001) Terrestrial ecoregions of the worlds: a new map of life on Earth. Bioscience 51(11): Aitchison JC, Ali JR, & Davis AM (2007) When and where did India and Asia collide? Journal of Geophysical Research 112(B05423). 3. Kumar P, et al. (2007) The rapid drift of the Indian tectonic plate. Nature 449: Meulenkamp JE & Sissingh W (2003) Tertiary palaeogeography and tectonostratigraphic evolution of the Northern and Southern Peri-Tethys platforms and the intermediate domains of the African-Eurasian convergent plate boundary zone. Palaeogeography, Palaeoclimatology, Palaeoclimatology 196(1-2): Janis CM (1993) Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annual Review of Ecology and Systematics 24: Whybrow PJ & Mcclure HA (1980) Fossil mangrove roots and palaeoenvironments of the Miocene of the eastern Arabian Peninsula. Palaeogeography Palaeoclimatology Palaeoecology 32(1980):

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