Saberes matemáticos ancestrales

5.1 INTRODUCTION

Observed biodiversity is the result of an interaction between rates of species origination and extinction. This interaction produces the myriad tree shapes that we see in species phylogenies. Quantifying the effects of speciation and extinction is a major goal of evolutionary studies, but distinguishing between the two can be difficult particularly as extinction is not independent of speciation. It would be ideal to compare biodiversity trends observed in molecular and paleontological datasets for the same lineage. However, the majority of molecular phylogenetic studies have been concerned with groups that have poor fossil records (Paradis 2004). In many cases robust unequivocal phylogenies are not available for fossil groups (Etienne and Apol 2009) due to the incompleteness of the fossil record and difficulties in species assignments (Kidwell and Flessa 1995; Cooper et al. 2006; Valentine et al. 2006). As a result there have been few direct comparisons between molecular and paleontological studies of evolution for the same group. In the absence of complete, directly comparable datasets, comparisons must be based on some amount of inference from each dataset. An eminently tractable means of comparing the patterns of evolution between paleontological and molecular data is through analysis of the of diversification rates inferred by the two data sets. The fossil record is often used for temporal calibration of molecular phylogenies for

subsequent analysis of the patterns of diversification. However, diversification rates have rarely been compared in equivalent molecular and paleontological datasets. Usually rates are inferred from one of these datasets and compared against a null model.

Methods for calculating origination and extinction rates are well established for both phylogenetic (e.g. Nee 2001; Nee 2006) and fossil (e.g. Foote 2000; Foote 2007) data. Estimates of speciation and extinction rates generated using these datasets form the basis of much research aimed at exploring the generation of biodiversity and are key to our understanding of the interface between micro- and macroevolution (e.g. Nee 2006; Mittelbach et al. 2007; Ricklefs 2007; McPeek 2008; Purvis 2008; Rabosky and Lovette 2008).

For some time speciation rates have been inferable by lineage through time (LTT) analysis of molecular phylogenies. More recently, the advent of modelling a birth/death process in the inference of molecular phylogenetics has enabled the estimation of extinction rates from molecular data (Nee 2001). While speciation rates estimated from fossil data are often more precise, rates inferred from molecular phylogenies can be correctly estimated despite considering only extant species (Paradis 2004). However, when extinction rates are high accurate

estimation of rates from molecular data is much less likely (Paradis 2004). A minimum of 15 species has been quoted as being sufficient for accurate estimation of the speciation rate in a clade; fewer than this will lead to an underestimate (Paradis 2004). However, most species in a genus are required for accurate

inference (Barraclough and Nee 2001) as missing species will cause a reduction in the inferred rate (Paradis 2004). Extinction rates appear to be well estimated from phylogenies when the clade size ranges from 10 to 20 taxa, but are not as accurate as rates estimated from fossil data and are under-estimated in most cases in simulation studies (Paradis 2004). Random extinction with a constant probability is expected to cause an apparent acceleration in speciation rate towards the present (Barraclough and Nee 2001).

The analysis of origination and extinction rates, sometimes referred to as

taxonomic rates, in the fossil record has a long history. Methods to calculate these rates have been reviewed by Raup (1985) and again by Foote (2000). The main

incomplete nature of the fossil record, difficulties with identification at the species level, and lineages that are found in only a single geological time span (singletons). Significant paleontological research has been devoted to accounting for

preservation and sampling bias in the fossil record (e.g. Crampton et al. 2003; Cooper et al. 2006; Crampton et al. 2006a). The problem of species identification has meant that the analysis of taxonomic rates in the fossil record has been based on higher-level groupings, genera and above (Jackson and Johnson 2001).

However, it is possible to derive species-level rates from data resolved to the genus level (Foote 2007). Accounting for singletons in a dataset has been shown to result in more accurate estimates of taxonomic rates (Foote and Sepkoski 1999; Alroy 2000). The large body of work devoted to the accurate estimation of taxonomic rates has highlighted some new potential problems. Origination (or speciation) rates may be more significantly distorted by incomplete preservation than

extinction rates as extinction events have a greater tendency to coincide with stages with high preservation probabilities (Foote 2001). Additionally, origination and extinction rates are unlikely to be constant over time. Studies show that origination rates vary less then extinction rates over short timescales, but over long time scales origination rates vary at least as much as extinction rates in marine invertebrate families (Kirchner 2002).

5.1.1 Alcithoe

The fossil record of the New Zealand volute lineage (tribe Alcithoini), represented in the modern fauna by the genus Alcithoe, has been the subject of study for over 100 years (e.g. Suter 1913; Marwick 1926; Dell 1978; Powell 1979). Volutes are distinctive large snails that that live on soft substrates that are suitable for fossil preservation. Extensive collections of extinct and dry extant specimens allow for an excellent picture of the presence of members of the group through the Cenozoic era (55 Ma until the present). The inference of a robust dated phylogeny for the

Alcithoe (previous chapter) now allows comparisons to be made between the molecular and paleontological data. While it would be ideal to compare the phylogenetic analyses of the two data sets, as has been discussed (Chapter 1) a paucity of discriminating morphological characters make inference of a complete phylogeny based on the fossil record difficult.

5.1.2 Systematics of the fossil Alcithoini

In an attempt to estimate the phylogenetic relationships of the higher order

groupings of the Alcithoini lineages an unofficial review of the generic relationships of many of the New Zealand fossil Volutidae was carried out (Beu, Maxwell, Cooper, Crampton and Marshall, unpublished) see Figure 5.1. This review suggested a revision of several generic relationships within the Alcithoini, and highlighted several affinities that some of the modern species have with other recognised genera. The absence of fossils of Mauira through the entire Oligocene suggests that the genus should be divided into two groups. One represents the true Mauira from the Eocene, the other encompasses the group of species currently recognised as Mauira from the Miocene. It was suggested that this group diverged from Alcithoe during the mid Miocene. It was recognised that the genera Spinomelon, Teremelon and Waihaoia share many characteristics and may represent a single lineage. Furthermore, despite the absence of these genera from the fossil record during the Pleistocene, it is possible that Alcithoe benthicola is derived from this lineage. This hypothesis is based on the presence of an apical spike on the protoconch of A. benthicola, a characteristic feature of Spinomelon and Waihaoia specimens (Alan Beu and Bruce Marshall, pers com.). Alcithoe is presumed to have diverged from the Spinomelon lineage during the Whaingaroan stage of the early Oligocene leading up to its first occurrence in the fossil record in the Duntroonian. A separate divergence from Spinomelon at a similar time led to the genus Metamelon, which is now considered to have a longer fossil history than is indicated in Beu and Maxwell (1990). Leporemax is thought to have diverged from Alcithoe sensu stricto during the Otaian (21.7 – 19.0 Ma), as the first fossils recognised as Leporemax appear in the Altonian. At the time of the revision (Figure 5.1), Alcithoe fusus was thought to be a modern example of Leporemax, and A. jaculoides could be an offshoot of the lineage. However, the taxonomic status of this sub-genus was questioned, as the number of specimens in collection has increased, the number of characters

supporting the separation of Leporemax has declined. Mauithoe is inferred to have been derived from Alcithoe in the mid Miocene at a similar time to the Miocene “Mauira” group. Finally, Iredalina mirabilis appears in the fossil record in the Nukumaruan, possibly immigrating from the region of South America (Figure 5.1).

FIGURE 5.1—Revised generic relations for the New Zealand Alcithoini. Dashed lines

indicate where unconfirmed fossil data exists. Dotted lines show the theoretical relationships between the genera. Putative generic affinities of some extant species are indicated. The stages of the New Zealand geological timescale are included (Wq – Haweran, Wc – Castlecliffian, Wn – Nukumaruan, Wm – Mangapanian, Wp – Waipipian, Wo – Opoitian, Tk – Kapitean, Tt – Tongaporutuan, Sw – Waiauan, Sl – Lillburnian, Sc – Clifdenian, Pl – Altonian, Po – Otaian, Lw – Waitakian, Ld – Duntroonian, Lwh –

Whaingaroan, Ar – Runangan, Ak – Kaiatan, Ab – Bortonian, Dp – Porangan, Dh – Heretaungan, Dm – Mangaorapan, Dw – Waipawan)

5.1.3 Species patterns relevant to modern taxa

There are several species-level patterns in the fossil record that are relevant to the interpretation of the modern taxa. These patterns in particular will be useful to compare with molecular data as they directly involve species that are tractable to molecular analysis. Beu and Maxwell (1990) recognise a morphological grade in the Leporemax lineage based on the decreasing prominence of costae in the taxa

involved. In this grade A.(L.) rugosa is ancestor to A.(L.) gatesi which is ancestor to A.(L.) brevis which gives rise to A.(L.) fusus. In particular these authors recognise a very gradual intergrade from A.(L.) brevis to fusus. However, the close relationship of A.(L.) brevis and fusus has been questioned (B. Marshall, pers. com).

Acknowledging that this gradient represents a progenitor/progeny species relationship leads to the conclusion that Alcithoe fusus belongs to a lineage of morphologically similar species that is at least 10 million years old.

Using the molecular phylogeny for the Alcithoe and drawing on data from the paleontological record of the New Zealand volutes I address the question; in the study of evolution are molecular and paleontological data comparable? More specifically, can a data from one discipline be used to test hypotheses arising from

data from the other? Or, do they provide complementary but distinct information? By comparing patterns and rate estimates of clade evolution derived from

molecular and paleontological data for Alcithoe, I will examine where the two datasets are concordant and where they are not. Finally I will show that it is appropriate to consider these datasets in parallel.

5.2 METHODS

Using values of B-D and D/B, estimated from molecular data, the approximate rates of speciation (B) and extinction (D) can be calculated. Bayesian phylogenetic inference under a birth-death model of clade expansion, or speciation, yields posterior statistics for the values diversification rate B-D and the extinction to speciation ratio D/B, which is a measure of the degree that by which the

diversification rate differs from a pure birth process. Larger D/B values indicate a greater deviance (Nee 2006). Values of B-D and D/B for the Alcithoe molecular phylogeny were obtained from the final analysis described in Chapter 4. As

described in Chapter 4, three internal nodes were calibrated using the fossil record of the species A. wilsonae, A. arabica and A. fusus. To investigate estimates of these values over shorter timeframes Bayesian analysis was carried out using nested subsets of the Alcithoe phylogeny. These analyses where carried out using BEAST v1.4.8 using model parameters identified in Chapter 4, with the exception of the tree root-height calibration. This calibration varied for each analysis as the oldest divergence in the taxa under examination decreased. Root node calibrations for each of the taxon subsets were set with lognormal priors that best approximated the mean and 95% HPD for the relevant node in the complete dataset. A lineage through time (LTT) plot was generated using the complete molecular phylogeny, but only considering the Alcithoe species. The number of branches was counted every two million years, beginning at 20 million years ago (Ma). The median node heights and 95% highest probability density (HPD) interval were considered in order to plot an estimated confidence interval for the LTT plot. Fossil occurrence data for the New Zealand volute tribe Alicthoini was extracted from Beu and Maxwell (1990). This data is based on first and last occurrence in the fossil record. Rates were derived from the fossil data using calculations for dynamic survivorship analysis and per stage rate estimates described in Foote and Miller (2007).

Due to different analyses providing estimates in different units the ratio of

extinction to speciation may be an appropriate way to compare values generated by different methods as used by Ricklefs (2007).

5.3 RESULTS

5.3.1 Patterns in molecular and paleontological datasets

Comparing the molecular phylogeny to the revised generic relationships (Figure 5.2) reveals several inconsistencies. However, the root of the molecular tree, representing the divergence of the Alcithoini tribe, is broadly consistent with the fossil data, based on the overlapping 95% highest probability density (HPD)

interval. However, given that only the upper third of the 95% HPD interval overlaps with the expected 50 - 55 Ma age of Alcithoe, there is a persuasive suggestion that the molecular data support a younger origin than the oldest currently recognised fossil for the group. The earliest divergence in the extant taxa shown in the

molecular phylogeny significantly post-dates the earliest recognised Alcithoe fossil. In addition, the diversification of the modern species, including A. fusus, is later than the implied origin of the Leporemax subgenus. As A. fusus is recognised as the type species for Leporemax, and given the close relationship of A. fusus to Alcithoe sensu stricto, it appears clear that Leporemax is a synonym of Alcithoe and fossil species assigned to Leporemax cannot be placed there. It is not yet clear if the fossil species currently recognised fossil Leporemax species truly represent a separate clade or are members of the Alcithoe s. str., additional morphological analyses will be required to clarify the affinities of these extinct species. Furthermore, the

inclusion of Alcithoe benthicola in the Spinomelon genus, as this genus is currently understood, is not supported by the molecular phylogeny. An interesting

coincidence of divergence times exists between the molecular based inference of the origin of the extant Alcithoe lineage and the fossil based inferences of divergence times of the Mauithoe and “Mauira” groups, all in the middle Miocene.

FIGURE 5.2— (facing page) Direct comparison of the molecular and paleontological

data for the tribe Alcithoini. Putative affinities of a selection of extant species to the recognised genera and the revised generic relationships are shown for comparison to the molecular data. Fossil occurrence for recognised Alcithoini species are shown, based on first and last occurrence. Living species of Alcithoe that are represented in the fossil record are marked with an asterisk. The time scaled dated molecular phylogeny is shown with the median node ages and 95% HPD intervals. The globally recognised Epochs are indicated and the stages of the New Zealand geological timescale are included (Wq – Haweran, Wc – Castlecliffian, Wn – Nukumaruan, Wm – Mangapanian, Wp – Waipipian, Wo – Opoitian, Tk – Kapitean, Tt – Tongaporutuan, Sw – Waiauan, Sl – Lillburnian, Sc – Clifdenian, Pl – Altonian, Po – Otaian, Lw – Waitakian, Ld – Duntroonian, Lwh – Whaingaroan, Ar – Runangan, Ak – Kaiatan, Ab – Bortonian, Dp – Porangan, Dh – Heretaungan, Dm – Mangaorapan, Dw – Waipawan)

A side-by-side comparison of the molecular phylogeny and a species level summary of the fossil record of the New Zealand Volutidae (Figure 5. 2) allows a

consideration of the stage-based, discontinuous paleontological data with

continuous relationships inferred by the molecular data. The continuous picture shows that diversification of a single lineage of the Alcithoini tribe, beginning in the early to middle Miocene, has led to all of the modern diversity. The fossil data shows that diversity in the Alcithoini lineage was relatively high in the early Miocene. However, by the middle Miocene the Alcithoini fauna is poorly

represented in the fossil record. Species diversity is again relatively high in the late Miocene, and extant taxa potentially originating at this time represent between 18 and 45% of the modern diversity. The majority of diversification leading to extant Alcithoe species, as inferred by the molecular data, has occurred in the Pliocene. Indeed, as much as 45% of the modern diversity originated in the last 2.5 million years. By contrast, no extinct species are seen in the fossil record from the same timeframe, likely due to the lack of fossil deposits representing deeper water faunas from this time.

When considering only the fossil record of Alcithoe species, the data shows that most extinct species occur in only one stage (Figure 5.2). Similar levels of diversity, as are seen in the modern taxa, are observed in the Altonain and Tongaporutuan stages. However, a conspicuous fossil gap in the middle Miocene, particularly the Lilburnian stage (15.1 – 12.7 Ma), masks the faunal turnover occurring around the time of the earliest divergence in the modern taxa. As has been discussed earlier (Chapters 2 and 3) fossil and molecular data are highly concordant in the inference of the time of origin of the species Alcithoe wilsonae. Much of the diversification of the extant Alcithoe has occurred in the last 2 million years.

5.3.2 Rates from different datasets

Bayesian estimation inferred a median diversification rate (B-D) for the complete molecular phylogeny of 0.0496. The median D/B value for the same analysis is 0.5671. This value infers a considerable departure from a pure birth process (where D = 0) indicating that, as expected, extinction has played a significant role in the evolutionary history of the New Zealand Volutidae. Using these values the calculated speciation rate is 0.1146 speciations Myr-1 _{and the extinction rate is}

0.0650 speciations Myr-1_{, for this phylogeny. As the extinction to speciation (D/B)}

ratio indicates, the extinction rate accounts for 57% of the speciation rate in the molecular data.

Proportional rates of speciation and extinction were calculated from the fossil record to compare with the molecular based estimates. These rates were based on the numbers of originations and extinctions observed in the species level summary of the Alcithoini lineage (Figure 5.2) over the time interval roughly equivalent to the molecular phylogeny (approximately 50 Ma and the present). The per-taxon

extinction rate is around 0.018 per million years, and the origination rate is approximately 0.02 per million years. Therefore in the fossil record the extinction rate is 90% of the speciation rate.

In order to incorporate the time frame between the origination of the Alcithoini tribe and the divergence of the modern Alcithoe species, the molecular analysis included out-group taxa. This time frame includes the Alcithoe stem lineage, and has clearly been dominated by extinction. However, the inclusion of out-group taxa in the molecular phylogeny is probably a source of significant error as they

significantly under-represent the taxonomic diversity that exists between the

ingroup and out-group. This error will have the effect of misleading the estimates of the B-D and D/B values, but its magnitude is unknown. To be able to include more of the timeframe that is effectively missing in the molecular phylogeny, sampling a taxon that diverged much closer to the root of the Alcithoini tribe would be

necessary. As such a sampling has not yet been achieved, we can only make