*Department of Biological Sciences and NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire;
Department of Entomology, The Natural History Museum, Cromwell Road, London
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Abstract |
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Introduction |
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One area that should benefit from this approach is the determination of how diversification rates have been affected by major climatic changes, in particular by climatic fluctuations during the Pleistocene. Many authors have argued that recurrent ice ages over the last 2.5 Myr increased speciation rates by promoting founder events (Hewitt 1999
) and the divergence of populations in isolated glacial refugia (Haffer 1969
). Key evidence for this hypothesis has been that pairwise DNA sequence divergences between closely related taxa often support a high frequency of species origins during the Pleistocene (Brower 1994
; Hackett 1996
; Roy 1997
). But other authors have argued that speciation rates declined during the Pleistocene (Zink and Slowinski 1995
), possibly because of increased mixing between populations (Coope 1979
). Also, the DNA evidence remains controversial (Klicka and Zink 1997
; Avise and Walker 1998
; Klicka and Zink 1999
). Demonstrating that there are large numbers of divergences consistent with Pleistocene origins does not prove that speciation rates increased at that time because we might expect most species to have had recent origins, even if speciation rates have remained constant (Avise and Walker 1998
; Klicka and Zink 1999
). To resolve this issue, we need to investigate the dynamics of diversification, comparing Pleistocene speciation rates with those observed before the onset of glacial cycles. The one previous study taking this approach concluded that speciation rates in 11 North American bird genera had declined rather than increased during the Pleistocene (Zink and Slowinski 1995
).
Here, we investigate recent diversification rates in the North American tiger beetles of the genus Cicindela, using a phylogenetic tree reconstructed from mtDNA that is densely sampled at the species level (A. P. Vogler, A. C. Diogo, and T. G. Barraclough, unpublished data). The genus Cicindela represents a spectacular radiation of insects, with around 130 species in North America and over 1,000 species found on all continents worldwide (except Antarctica, Pearson 1988
). All species are sleek, raptorial predators, relying on fast locomotion (both in flight and on foot) and large mandibles to actively chase down a variety of arthropod prey. They have been well studied, particularly in North America, where their taxonomy, ecology, and geographic distributions are better known than in most other insect groups. Authors have proposed scenarios for the origin of tiger beetle species since the early days of their study (Leng 1902
) and invariably phrase the speciation history of subgroups in the context of glaciation events (Freitag 1965
; Rumpp 1967
; Willis 1967
; Acorn 1992
). Because of the extreme scarcity of fossil remains (less than 10 fossils are known from North America, none more than 20,000 years old; Nagano, Miller, and Morgan 1982
), attempts to investigate speciation and extinction in the group rely almost exclusively on phylogenetic data (Vogler and DeSalle 1993
; Vogler, Welch, and Barraclough 1998
; Barraclough, Hogan, and Vogler 1999
; Barraclough and Vogler 2000
; Morgan, Knisley, and Vogler 2000
).
We extend recent methods to estimate average diversification rates among the North American Cicindela and to investigate how these rates have changed over time, in particular during the Pleistocene. Our analyses use dates estimated from the mtDNA tree and calibrated using biogeographic evidence. Glacial cycles are thought to have started in North America around 2.5 MYA, with increased intensity over the last 0.7 Myr (Webb and Bartlein 1992
). Therefore, if glaciation increased speciation rates, we expect to observe an increase in per-lineage speciation rates around that time. But other processes can lead to similar patterns, for example, a constant background extinction rate is expected to cause an apparent acceleration in diversification rate toward the present (Harvey, May, and Nee 1994
; Nee et al. 1994
). We use statistical models to distinguish these alternatives and demonstrate a weak increase in Cicindela speciation rates within the last million years.
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Materials and Methods |
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Estimating the Relative Ages of Nodes from Sequence Data
We used the sequence data to estimate relative node ages for the phylogeny of Cicindela. First, branch lengths were fitted to the maximum parsimony tree of the full analysis (Vogler, Diogo, and Barraclough 2001
) using maximum likelihood (ML) implemented in PAUP* 4.0 (Swofford 2001
). The HKY85 model (transition-transversion ratio estimated from the data) with gamma-distributed rate variation among sites was chosen as significantly better than simpler models based on log likelihood ratio tests (Goldman 1993
). Fitting more complex models led to improved likelihoods, but the branch lengths were highly correlated with those obtained under the chosen model (results not shown).
Likelihood ratio tests between rate-constant and rate-variable models revealed significant deviation from a molecular clock (Felsenstein 1981
). Character-based methods are available for correcting rate variation among lineages (Thorne, Kishino, and Painter 1998
; Huelsenbeck, Larget, and Swofford 2000
), but implementation is still difficult for large matrices. Instead, we used two computationally simpler methods. First, we used Sanderson's nonparametric rate smoothing algorithm (NPRS) to estimate relative node ages from the unconstrained ML branch lengths (Sanderson 1997
). The algorithm does not assume a strict molecular clock, simply that neighboring branches on the tree tend to have similar rates. Second, we fitted ML branch lengths under the chosen substitution model but assuming a molecular clock. Although our data deviate from a strict clock, there is a strong linear relationship between unconstrained and clock branch lengths (r2 = 0.88), suggesting that rate variation may not affect our estimates of node ages too greatly (Losos and Schluter 2000
). We perform all analyses on NPRS and ML clock estimates of node ages in turn. Details of calibrating the relative ages in terms of millions of years are provided in the results section.
Estimates of relative node ages using both methods will have associated errors caused by our finite sample of nucleotide characters. To assess the level of error, we generated 20 resampled bootstrap data matrices using the SEQBOOT program in PHYLIP, Version 3.573 (Felsenstein 1995
). Each matrix was imported into PAUP* 4.0 and the maximum parsimony tree found by heuristic search (100 random addition replicates, tree bisection-reconnection [TBR] swapping, maximum of five trees held at each stage). Node ages were then fitted to one of the shortest trees obtained for each bootstrap replicate, using the procedures outlined previously. Analyses outlined subsequently were repeated on each of the resulting ultrametric trees to assess the effects of errors in topology and branch lengths caused by having a finite sample of characters.
Missing Taxa
Subsequent analyses assume that all extant species within the assemblage have been sampled in the phylogeny. To examine the possible effects of missing species, we placed all the missing North American species described in Boyd (1982)
in their most likely place on the tree on the basis of taxonomic accounts (Cazier 1954
; Rivalier 1954
; Boyd 1982
). A further problem is that taxonomic effort has been greater in the United States and Canada than in Mexico. One unpublished checklist of Mexican species describes 16 additional species not included in the Boyd (1982) checklist (W. Sumlin, personal communication), mostly the result of upgrading existing subspecific taxa and new discoveries in previously unsampled areas. Hence, although the alpha taxonomy of the Mexican taxa remains unstable, we also added these presently "undescribed" species in their most likely place on the mtDNA tree. The result is a tree containing 146 species. For subsequent analyses we removed the four species that are members of predominantly South American clades from our original tree because these clades are very incompletely sampled in our mtDNA tree. All analyses were repeated with this tree as well as our original mtDNA tree. This treatment cannot tell us the relationships we would obtain if missing taxa had been included in our matrix, but we use it to give some indication of how missing taxa may affect our analyses. The modified tree is available online. Note that we have no information for branch lengths connecting the added species. Instead, we assigned nodes to be half way along the branch to which each species was added (Losos 1990
). This would tend to be conservative with respect to detecting a recent increase in the apparent diversification rate.
Estimating Diversification Rates
We plot the log of the number of lineages against the branch length distance from the root node (for the ultrametric trees obtained by NPRS and ML clock). Because the North American Cicindela are not monophyletic, we consider diversification rates only over the time interval since the most recent, first within-continent split for a radiation confined to the continent (see fig. 1
). Under a constant speciation rate model we expect a straight line with slope b, the speciation rate. If there has been a recent increase in the speciation rate caused by the onset of glacial cycles, then we expect an increase in slope at around 2.50.7 MYA (Klicka and Zink 1999
). If there has been a constant background extinction rate, d, then we expect an apparent acceleration in diversification rate toward the present, with the slope changing from b - d to b, starting at around 1/(b - d) Myr before the present (Harvey, May, and Nee 1994
).
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To test for significant departures from the constant speciation rate model we follow Pybus and Harvey (2000)
. Their statistic,
, compares the relative positions of nodes in a phylogeny to those expected under a constant speciation rate model (see also Zink and Slowinski 1995
). This can be generalized as described subsequently. For a time window starting at time 0 with m species and finishing at time t with n species and where gm, gm+1, ...,gn are the internode distances during the time period as shown in figure 1
, the statistic is equation (1)
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Under a constant speciation rate model, the statistic follows a standard normal distribution. Positive values signify that nodes are closer to the tips than what is expected under the constant speciation rate model, i.e., there has been an apparent increase in diversification rate toward the present. Negative values signify an apparent deceleration. Therefore, the null hypothesis of constant b cannot be rejected at 5% level in a two-tailed test if -1.96 < < 1.96. Hence, we calculated
for the time window since the most recent invasion by a major group to test whether net diversification rates changed over time.
An increase in the speciation rate during the Pleistocene would lead to a significant positive value of . But a constant rate of background extinction could also cause a significant increase in the apparent diversification rate toward the present. To distinguish these alternatives we performed the following test (see also Paradis 1997
; Emerson, Oromi, and Hewitt 2000a
, 2000b
). Under a constant speciation and extinction rate model of clade growth, the likelihood of each internode distance gi is given by
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Our analyses consider the average diversification rates across at least four independent radiations within North America. To test for variation among them, we repeated our analyses on each of the major subgroups in turn. Apart from estimating b for each clade, we also tested for significant differences in b among groups. For each group we multiplied each internode distance by the number of lineages present during that internode, i.e., we calculated igi for all internodes. Under the constant speciation rate model, these transformed internode distances are expected to be constant and equal to 1/b (Purvis, Nee, and Harvey 1995
; Nee 2001
). Hence, we tested for significant differences among clades using an ANOVA with subgroup as the single factor and transformed internode distances as the data. For each clade, we also tested for significant departures from the constant speciation rate model, using the
statistic.
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Results |
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Because the North American Cicindela are not monophyletic (see Materials and Methods), the average rates of diversification were only calculated across subclades representing radiations confined to this continent. These clades are shown in figure 2 and include four major subgroups: the subgenera Cicindela s.s., Cicindelidia, Ellipsoptera, and a clade confined to ocean beaches and salt flats comprising the subgenera Habroscelimorpha, Opilidia, Eunota, and the divergent Cicindelidia trifasciata (hereafter referred to as "Beach clade," Vogler, Diogo, and Barraclough 2001
). Microthylax was also included for the overall analysis of diversification rates but was not included in the separate analyses of subclades (see subsequently) because the number of species is too small to allow an accurate estimation. The recent South American invaders were not included in our analyses of diversification rates.
Cicindela s.s. probably comprises three independent radiations within North America (Vogler, Diogo, and Barraclough 2001
) and includes the most recent colonization leading to a major in situ radiation in North America, the Cicindela s.s. group 2. The earliest within-continent split in this group is estimated at 5.6 MYA in the NPRS tree. Hence, we consider diversification rates from this date. Figure 3
shows the lineage-through-time plot for the North American Cicindela sampled in our tree over the last 5.6 Myr. The plot obtained when missing species were added to the phylogeny is superimposed. The pattern observed is that of a roughly linear increase on the semi-log plot but with some indication of acceleration in rate toward the present, which becomes more marked when missing species are added.
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These findings were confirmed by comparing the likelihoods of the data under the three models of diversification rates (table 3 ). When only species sampled in our mtDNA survey were included, the best model for the ML clock dates was the constant speciation rate model and that for the NPRS dates was, marginally, a step-model with a decrease in the speciation rate shortly after the start of the time-window (at about 5 MYR). When missing species were added, both ML and NPRS dates were best explained by a step-model with an 80% increase in the speciation rate at 1 MYR, but this was only marginally better than the constant speciation and extinction rates models (with extinction fairly high relative to speciation, d/b > 0.7). The favored model is consistent with the predictions of the glacial speciation model that speciation rates increased between 2.5 and 0.7 MYR.
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Tables and figures comparing diversification among the four major North American subgroups, Cicindela s.s., Cicindelidia, the Beach clade, and Ellipsoptera, are provided in the electronic appendix. The ANOVA of transformed internode distances using NPRS dates revealed little difference in the net diversification rate among subgroups, becoming marginally significant only when missing species are added (F = 3.8, P < 0.05). The differences among groups were more significant using ML clock dates (sampled taxa, F = 3.2, P < 0.05; missing species added, F = 6.8, P < 0.01). The main trend is for a lower diversification rate in the Beach clade compared with the other three groups. The statistics for each group revealed little significant departure from the constant speciation rate model, except for an increase toward the present in Cicindela s.s. using the ML clock dates. Interestingly, Cicindela s.s. and Ellipsoptera, both of which have a northerly distribution in the continent, displayed more positive values of
than did the other two clades. The Beach clade displayed a nonsignificant decline in diversification rates toward the present, and Cicindelidia displayed a decline that became a slight increase when missing species are added.
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Discussion |
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How does this compare to the typical diversification rates in insects and other groups? Mayhew (2002)
estimated rates in insect orders from fossil dates, ranging from 0.008 to 0.06 species/Myr, but the wider taxonomic scale limits the usefulness of direct comparison. McCune (1996)
cites speciation rates in Hawaiian insects that range from 0.66 to 1.21 species/Myr on the basis of the numbers of extant species and the geological age of the oldest extant island in the Archipelago. But if the taxa first colonized older but now extinct islands, these estimates could fall by up to one-tenth (McCune 1996
). A few studies have used the methods we followed to estimate diversification rates in other groups, for example, between 0.09 and 0.34 for a range of primate clades and 0.56 for Hawaiian silversword plants (Purvis, Nee, and Harvey 1995
; Baldwin and Sanderson 1998
). More studies are needed to establish typical diversification rates in different organisms, but compared with present studies the North American Cicindela provide no indication of unusually high diversification rates.
Our results provide some evidence for the effects of Pleistocene glaciations on tiger beetle diversification. When missing species were added to our mtDNA tree, we observed a weakly significant twofold increase in the net diversification rate within the last million years, consistent with a response to the increased intensity of glacial cycles in the late Pleistocene (Webb and Bartlein 1992
). Previous work showed that the North American tiger beetles have experienced major range movements (Barraclough and Vogler 2000
), and the effects of climate change on species ranges would be a likely cause for the increased speciation rate. But the alternative explanation that speciation rates have been constant over time but with a high background extinction rate was only slightly less favored. This shows that it can be difficult to distinguish alternative explanations for a given pattern of diversification even with a sample size of over 70 nodes, large potential effect sizes (i.e., doubling in speciation rate or d > 0.7b), and efficient statistical methods (Barraclough and Nee 2001
).
The results on how diversification rates changed over time were sensitive to our reconstruction of node ages from the mtDNA data. The increase in diversification toward the present was strongest using ML clock dates: with NPRS dates there was only a weak evidence to reject the constant speciation rate model, and the trends were sensitive to resampling. This arose because NPRS stretched out the ages of clades with low sequence divergence among species, whereas the clock method stretched internal branches and left terminal clades with shorter branches. Comparisons with unrelated data suggest that the direction of bias varies among data sets (T. G. Barraclough, unpublished data). More work is needed to evaluate these methods, in particular how they affect the distribution of ages obtained for a given data and how well they perform when their assumptions are not met. Although the ML clock method assumes an unjustified molecular clock, the assumptions of NPRS (i.e., rates change smoothly across the tree) may not be any more justified. Because both methods make unjustified assumptions, it is not clear which method will provide the best estimates even though NPRS nominally allows for rate variation. We believe that character-based approaches that incorporate rate variation among lineages will be the best solution (Thorne, Kishino, and Painter 1998
; Huelsenbeck, Larget, and Swofford 2000
) once methods that can be applied to large data sets become available.
Missing species had a sizeable effect on the change in diversification rates over time. The increase in rates was only found when missing species were added to our mtDNA tree. Although we know that at least 20 recognized North American Cicindela species are missing from our tree, we can only guess what the tree would have been if mtDNA from those species had been sampled. Simulations suggested that the ML clock results were robust to this uncertainty, but the weaker NPRS results were sensitive to the location of missing species.
More fundamentally, our study assumes that currently recognized taxonomic species correspond to evolutionary units. Tiger beetle species have been described mostly on the basis of evolutionarily labile traits, such as elytral coloration and body proportions, which may indicate substantial historical divergence in some cases but not others (Morgan, Knisley, and Vogler 2000
). Although in the present study practical limitations of sampling all species in the region made it necessary to follow the taxonomy, future studies at the population-species boundary in representative Cicindela are needed to justify this approach. Our results show how sensitive the analyses can be to departures from full sampling of a lineage; therefore, reliably identifying and sampling all the lineages within a clade is vital for this kind of study (Avise 2000
; Barraclough and Nee 2001
).
Finally, note that we compared three simple diversification models for the North American tiger beetles, but other scenarios could lead to similar patterns. For example, if a mass extinction event occurred 1 MYA, perhaps triggered by changes in glacial cycles, the expected pattern is for a change in the slope on the lineages-through-time plot at the time of the event (Harvey, May, and Nee 1994
; Kubo and Iwasa 1995
). Alternatively, if newly formed species have a higher risk of extinction than do older species, perhaps because their geographic ranges tend to be smaller, then this could lead to a shorter lag between speciation and extinction than in the constant extinction rates model. Both scenarios could lead to similar quantitative predictions to those of the Pleistocene speciation model. But although it is impossible to pin down a single explanation for the observed patterns, clearly our results reject the hypothesis that speciation rates declined during the Pleistocene because of mixing of populations in a dynamically changing landscape. Similar conclusions have been obtained from population studies in other insect groups (Hewitt 1999
; Knowles 2001
).
In conclusion, our study estimated diversification rates within an insect group from phylogenetic data and found marginal evidence for a late Pleistocene increase in the net diversification rate. Application of similar methods in a range of groups could provide critical insights into the effects of Pleistocene climate, and environmental change more generally, on diversification rates. Successful applications in the future will depend on robust methods for dating phylogenetic trees and on establishing the evolutionary status of taxonomically recognized species, a key assumption of studies of this kind.
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Supplementary Material |
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Acknowledgements |
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Footnotes |
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Keywords: diversification rates
speciation
extinction
tiger beetles
Pleistocene
Address for correspondence and reprints: Timothy G. Barraclough, Department of Biological Sciences, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK.> t.barraclough{at}ic.ac.uk
.
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