Implications of phylogeny reconstruction for ostracod speciation modes in Lake Tanganyika

Implications of Phylogeny Reconstruction for Ostracod Speciation Modes in Lake Tanganyika L.E. P A R K a n d K . F . D O W N I N G I. II.

III. IV.

V. VI.

VII.

Summary .................................................................................................... Introduction ............................................................................................... A. Biological Diversification in Lake Tanganyika .................................. B. Ostracods in Lake Tanganyika .......................................................... C. Speciation Models in Ancient Lakes .................................................. D. The Ostracod Genus Gomphocythere ................................................. Study Objectives ......................................................................................... Methods ..................................................................................................... A. Taxa and Characters .......................................................................... B. Phylogeny Reconstruction .................................................................. Results ........................................................................................................ A. Phytogenetic Patterns ......................................................................... Discussion .................................................................................................. A. Speciation Model ................................................................................ B. Speciation in the Tanganyikan Basin ................................................. C. The Single Invasion Scenario ............................................................. D. The Multiple Invasion Scenario ......................................................... E. Fluctuation in Lake Levels ................................................................. F. Tempo and Mode of Gomphocythere Speciation ............................... Conclusions ................................................................................................ Acknowledgements..................................................................................... References ..................................................................................................

I.

303 304 304 305 305 307 308 310 310 310 313 313 316 316 320 321 321 321 322 323 323 324

SUMMARY

Speciation in the East A f r i c a n lakes has been r e m a r k a b l e a n d has resulted in m a n y endemic species flocks, consisting o f several to h u n d r e d s of species. Lake T a n g a n y i k a , in particular, s u p p o r t s one o f the most diverse f a u n a s of any lake system. The origin of the T a n g a n y i k a n fish a n d g a s t r o p o d species flocks has been a t t r i b u t e d to divergence of p o p u l a t i o n s t h r o u g h the d e v e l o p m e n t of barriers to interbreeding, such as the f o r m a t i o n of separate lakes or h a b i t a t f r a g m e n t a t i o n within subregions of a single lake d u r i n g m a j o r falls in lake level. Similar speciation m e c h a n i s m s m a y have been i m p o r t a n t in the history of the diverse ostracod species flocks of Lake T a n g a n y i k a . A D V A N C E S IN E C O L O G I C A L R E S E A R C H VOL. 31 ISBN 0+12-013931-6

Cop)right + 2000 Academic Press All rights of reproduction in any form reserved

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L.E. PARK and K.F. DOWNING

In order to test hypotheses concerning character evolution and speciation patterns in this group, a phylogenetic analysis was conducted of the ostracod clade Gomphocythere. This analysis yielded high levels of homoplasy (CI = 0.56), permitting the development of a qualitative model to explain the observed phylogenetic patterns. This model considers two major speciation scenarios. The first involves a hypothetical radiation of a "parent" species and "daughter" species that evolve in a single lake system, taking advantage of available niche space. The resulting pattern is one with each daughter species evolving into its own niche space. In contrast, a scenario of multiple radiations from two lakes or lake sub-basins, with species brought together via a serendipitous invasion, or from water-level fluctuations having caused lakes to join together, suggests a complex phylogenetic reconstruction that could account for the high level of homoplasy seen in the analysis of Gomphocythere in Lake Tanganyika. Phylogeny reconstruction of the Gomphocythere species flock of Lake Tanganyika and the high homoplasy frequency revealed in this study support the importance of multiple radiations as a primary speciation mechanism in this ancient lake system. II.

INTRODUCTION

A. Biological Diversification in Lake Tanganyika The East African lake system has long been known as a site of megadiversity (sensu Mittermeier, 1988; Mittermeier and Werner, 1990), particularly with respect to the large, endemic species flocks that originated within several lakes in this geographical area (Coulter, 1991, 1994; Sturmbauer and Meyer, 1992; Snoeks et al., 1994; Rossiter, 1995). For example, almost 190 cichlid fish species (over 180 of which are endemic), 68 gastropod species (45 of which are endemic) and 80 ostracod species (almost all of which are endemic) have been described from Lake Tanganyika alone. For all of these groups, the given numbers are underestimates and many newly discovered taxa await formal description (e.g. see Snoeks; Michel; West and Michel, this volume). These speciose faunas provide excellent material for studies of diversification processes and diversity changes of endemic organisms over time. Analyses of cichlid fishes (Fryer and Iles, 1972; Sturmbauer and Meyer, 1992; LoweMcConnell, 1993; Sultmann et al., 1995; Verheyen et al., 1996; Rossiter and Yamagishi, 1997; Mayer et al., 1998) and thiarid molluscs (Cohen and Johnston, 1987; Michel et al., 1992) show that diversification patterns are often linked to environmental differences, and to incidences of multiple invasions and subsequent radiations in the lake. Whether or not similar patterns of evolution have produced the diversity observed in the lesser known groups

OSTRACOD SPECIATION MODES IN LAKETANGANYIKA

3(15

found in these lakes, such as the ostracods, can be tested through analyses of their phylogeny.

B. Ostracods in Lake Tanganyika Eighty described ostracod species, assignable to 25 genera, have been found in Lake Tanganyika. Almost all of these species are endemic to the lake (Rome, 1962) and provide an excellent means for studying diversification processes and diversity changes of endemic organisms. Most of them belong to three families, the Candonidae, the Cytherideidae and the Limnocytheridae. The genus Gomphocythereis a member of the Limnocytheridae. Very little is known about speciation patterns of ostracods in the African lakes, although it has been widely speculated that allopatric speciation in isolated basins during low lake levels may contribute to their radiation (e.g. Martens, 1994). However, little work has been done on documenting and developing phylogenetically based speciation models for any ostracod clade in any African lake system.

C. Speciation Models in Ancient Lakes Species flocks in ancient lakes in general, and Tanganyika in particular, have originated in various ways that may be taxon dependent. However, two basic patterns have emerged from studies of fishes and invertebrates. In some cases, species closely resembling the ancestral taxa are extant in the rivers, ponds and lakes surrounding the lake basins, and the invading species appear to have given rise to a monophyletic flock within the lake. In other cases, there is evidence of multiple radiations, with subsequent radiations either establishing themselves along with older ones or replacing them. In the latter case, some of the older radiations have suffered catastrophic extinctions either by repeated desiccation (e.g. Lakes Turkana and Victoria) or through volcanic eruptions (e.g. Lake Kivu) (Eccles, 1984; Coulter, 1991; Kolding, 1992; Bootsma and Hecky, 1993; Coulter, 1994). Two types of barrier to gene flow have been proposed as possible mechanisms which act to promote allopatric speciation within lakes. Extrinsic barriers involve the physical features of the lake environment, including lakelevel changes that can result in the development of isolated basins, and therefore include geographical barriers, as well as intrabasinal differences in temperature, light, pressure, density, water chemistry and substrate (Smith and Todd, 1984; Mayr, 1984; Coulter, 1994). Lake Tanganyika has been separated into isolated sub-basins throughout its history during times of low lake-level stand (c. 35 000-15 000 years bp, 16 000 14 000 years bp and 3500-1400 years bp) (Haberyan and Hecky, 1987; Scholz and Rosendahl, 1988; Tiercelin and Mondeguer, 1991) (Figure 1) and it has been speculated that these level fluctuations have had a profound effect on speciation of littoral cichlid fish

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OSTRACOD SPECIATION MODES IN LAKE TANGANYIKA

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(Coulter, 1994). Whether these same conditions also had a major effect on ostracod speciation, and were a more important factor than disjunct shorelines, substrate barriers to dispersal, or differences in water quality or chemistry, remains unknown. Intrinsic or biotic barriers are those that include characteristics of the organisms themselves, such as errant homing behaviour in fish (Horrall, 1981), food preference (Smith, 1987), colour preference (McKaye et al., 1984) and brooding mechanisms (Cohen and Johnston, 1987). Although it is possible to observe potential barriers to gene flow between extant populations in lakes, trying to establish the historical development of a barrier or sequence of barriers that actually resulted in speciation events is much more difficult.

D. The Ostraeod Genus

Gomphocythere

The genus Gomphocythere is a diverse taxon whose individual members show specificity to various environmental conditions, such as substrate and depth, making it an ideal group in which to document and understand diversification processes of ostracods in Lake Tanganyika. Fourteen described species of Gomphocythere can be found today in Africa and parts of the Middle East (e.g. Israel) (Figure 2). The sister or subgroup taxon, Qvtheridella, is found in South America, North America and Australia, whereas Gomphodella is restricted to Australia. The distribution of Gomphocythere in East African lakes is poorly understood. Several species appear to be endemic to individual, large, inland lakes; however, there are also widespread species that can be found in other lakes throughout Africa (Sars, 1924; Rome, 1962: Martens, 1990). In Lake Tanganyika Gomphocythere is represented by five described endemic species: G. alata, G. cristata, G. curta, G. lenis and G. simplex (Rome, 1962), and four additional, as yet formally undescribed species: G. "coheni'" n. sp., G. "downingi" n. sp., G. "wilsoni" n. sp. and G. "'woutersi'" n. sp. (Park and Martens, unpubl.) (Table 1). Despite their diversity, Rome (1962) is the only previous author to address specifically the taxonomy of Gomphocythere species in Lake Tanganyika. Gomphocythere species occur throughout the Tanganyikan basin, with certain species being more widely distributed and locally abundant than others. While certain species may be concentrated in a single sub-basin, no species is strictly limited to any sub-basin (Park, 1995). All members of the genus Gomphocythere are brooders, but the dispersal ability of this group is not well known; indeed, whether brooding organisms are better or poorer dispersers is still a point of contention (Fryer, 1996; Horne et al., 1998). For Tanganyikan Gomphocythere species, the action of water currents or fish migration may be a major factor influencing dispersal. The ostracods' small size may also contribute to their dispersal ability, as they can be carried throughout the

308

L.E. PARK and K.F. DOWNING

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Distribution of

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Fig. 2. Distribution map of Gomphocythere species in Africa. The numbers indicated on the diagram represent the following species: 1, Gomphocythere aethiopis; 2, G. alata; 3, G. angulata; 4, G. angusta; 5, G. capensis; 6, G. eristata; 7, G. eurta; 8, G. expansa; 9, G. lenis; 10, G. obtusata; 11, G. ortali; t2, G. pareedilatata, 13, G. simplex; 14, G. "'coheni" n. sp.; 15, G. "'downingi" n. sp.; 16, G. "wilsoni" n. sp.; 17, G. "'woutersi" n. sp.

lake by many different agents. It has been speculated that the distribution of the various species is related more to niche specifications and population dynamics than to radiations in different sub-basins, such as would occur through isolation owing to lake-level fluctuations (Cohen, 1995). Only a phylogenetic analysis, such as the one used here, can elucidate such a pattern. III.

STUDY OBJECTIVES

The primary purpose of this study was to document the phylogenetic pattern of one group of ostracods, Gomphocythere, in Lake Tanganyika, and to use that reconstruction to delimit the speciation patterns of the clade, thus providing a model for speciation of ostracods in large rift lakes. Despite the ostracods

OSTRACOD SPECIATION MODES IN LAKE TANGANYIKA

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Table 1

Taxonomy of species used in this analysis, including the four newly designated species endemic to Lake Tanganyika Subclass Ostracoda, Latreille, 1806 Order Podocopida, Mfiller, 1894 Suborder Podocopa, Sars, 1866 Superfamily Cytheracea, Baird, 1850 Family Limnocytheridae, Klie, 1938 Subfamily Timiriaseviinae, Martens, 1995 Tribe Cytheridelli, Danielopol and Martens, 1990 Genus Gomphocythere, Sars, 1924 Gomphocythere aethiopis, Rome, 1970 Gomphocythere alata, Rome, 1962 Gomphocythere angulata, Lowndes, 1932 Gomphocythere angusta, Klie, 1939 Gomphocythere capensis, MOller, 1914 Gompho~Tthere n. sp. "'coheni", Park and Martens, unpubl. Gompho~Tthere cristata, Rome, 1962 Gomphocythere curta, Rome, 1962 Gomphocythere n. sp. "downingi", Park and Martens, unpubl. Gomphocythere expansa, Sars, 1924 Gomphocythere lenis, Rome, 1962 Gomphocythere obtusata, Rome, 1962 Gomphoo,there ortali, Rome, 1962 Gomphoo'there parcedilatata, Rome, 1977 Gomphoo'there simplex, Rome, 1962 Gomphocythere n. sp. "wilsoni", Park and Martens, unpubl. Gomphocvthere n. sp. ~'woutersi", Park and Martens, unpubl. Genus Cytheridella Daday, 1905 Cytheridella chariessa, Rome, 1977 Subfamily Limnocytherinae, Klie, 1938 Tribe Limnocytherini, Klie, 1938 Genus Lhnnocythere, Brady, 1867 Lhmmcythere thomasi, Martens, 1990 Genus Leucocythere, Kaufmann, 1892

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L.E. PARK and K.F. DOWNING

being one of the better studied and most diverse taxonomic groups within the lake, only one group, the Megalocypridinaea, has had a phylogenetically derived hypothesis presented (Martens and Coomans, 1990). However, their study was not a quantitative cladistic analysis using Hennigian principles, and the present chapter is the first such cladistic approach towards investigating any ostracod group in the East African rift lakes.

IV.

METHODS

A. Taxa and Characters This analysis includes 16 Gomphocythere species from Lake Tanganyika and elsewhere in Africa, including the West Transvaal region (Republic of South Africa), the Ethiopian rift lakes, and Lakes Albert, Kivu and Turkana. The study used all known Gomphocythere available from the authors' own collections, collections of the Royal Belgian Institute of Natural Sciences and those documented in the literature. The species from Lake Tanganyika are Gomphocythere alata, G. curta, G. cristata, G. lenis and G. simplex, and the new species Gomphocythere n. sp. "coheni", G. n. sp. "downingi", G. n. sp. "wilsoni" and G. n. sp. "woutersi". Species from outside Lake Tanganyika are G. aethiopis, G. angulata, G. angusta, G. capensis, G. obtusata, G. ortali and G. parcedilatata. Outgroups, Cytheridella chariessa, Limnocythere dadayi and Leucocythere sp., were chosen from the family Limnocytheridae (Table 1). Characters for phylogenetic analysis were based on homologous structures and are coded as a numeric or alphabetic symbol that represents a particular character state (Wagner, 1989; Pogue and Mickevich, 1990). In total, 44 characters were defined and coded for all 19 taxa in the analysis (Appendix I). Similar numbers of hard-part characters (21) as well as soft-part characters (23) were identified for the composite analysis, using male and female data sets separately to avoid the problems caused by sexual dimorphism (Figure 3, 4). The complete matrix showing the presence and absence of characters and multistate values is given in Appendix I. Nine of 15 multistate characters were then coded, ordered as if they had successively additive states. Separate analyses were carried out for data sets with all unordered characters, and with the multistate characters that were coded as ordered.

B. Phylogeny Reconstruction The computer program PAUP (Swofford, 1998) was used to compute the most parsimonious tree from a character set of the 44 characters. Two types of run were undertaken. In the first runs, any change from one state to another was counted as one step. In subsequent analyses, nine characters were redefined as

OSTRACOD SPECIATION MODES IN LAKE TANGANY1KA

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c

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F

Fig. 4. Drawings of soft-part morphologies of Gomphocythere "downingi" n. sp. (A) Antennula, (B) antenna, (C) maxillula, (D) mandibula, (E) P3-walking limb, (F) hemipenis of male. Limb terminology follows Broodbakker and Danielopol (1982).

OSTRACOD SPECIATION MODES IN LAKE TANGANYIKA

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making the initial trees produced by P A U P unrooted. Since the outgroup taxa are included in the PAUP parsimony analysis, the assumption of monophyly of the ingroup is tested in the analysis. The trees were then rooted using outgroup analysis (Maddison, 1991). The computer program MacClade (Maddison and Maddison, 1992) was used to explore equally parsimonious character distributions within the minimal-length topology discovered by PAUP. Trees were compared with respect to their phylogenetic structure and then compared with trees produced with characters that were randomized over the taxa I.ve,.~ Archie. 1989).

V.

RESULTS

Using heuristic and branch and bound searches conducted with the phylogenetic reconstruction program, five trees of 99 steps were found (('1 = 0.56) (Figure 5). The skewness of tree-length distribution and permutation tests revealed significant phylogenetic structure in the data. Nodes were supported by one to 10 character state changes and these character changes were sometimes reversed or paralleled elsewhere, accounting for much of the homoplasy in the reconstructions. Additional analyses removing the more homoplastic characters (12 characters, defined as CI < 0.5) failed to improve the resolution markedly. Therefore, it was determined that the favoured tree structure can be supported even without the homoplastic characters. Gomphocythere was monophyletically distributed on the tree, with two major subclades being supported in each reconstruction: subclade A (G. aethi¢q~is, (;. obtusata, G. angulata, G. n. sp. "wilsoni'" and G. n. sp. "'downingi") and subclade B (G. alata, G. cristata, G. n. sp. "coheni", G. n. sp. "woutersi". (;. an,~usta, G. simplex, G. curta and G. lenis) (Figure 5). A majority rule consensus tree yielded a single phylogeny in which the monophyly of Gomphocyther~ ~ is supported, but the monophyly of a Tanganyikan endemic Gomphocythere clade is not (Figure 5).

A. Phylogenetic Patterns 1.

hTterlake Distribution

A plot of occurrence data for Gomphocythere in Africa showed no congruence between species distribution and phylogeny (Figure 5), and many geographically distant lakes share similar Gomphocythere species. This may be an artefact of the inadequate sampling of the ostracod faunas of many of the East African lakes but, even so, those species known do not support the hypothesis that there is a congruence between Gomphocythere phylogeny and species distribution in adjacent African lakes. For example, Lakes Kivu, Tanganyika

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Fig. 5. Majority-rule tree of the five most parsimonious reconstructions using unordered characters. The five initial trees have 99 steps, CI = 0.56, HI = 0.44, RI = 0.63 and three islands. Endemic Tanganyikan Gomphocytherespecies have been mapped onto the majority consensus tree. Note that endemics do not occur within a monophyletic, Tanganyikan clade.

OSTRACOD SPEC|ATION MODES IN LAKE TANGANYIKA

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and Victoria, which are adjacent to one another, do not share any of the same Gomphocythere species (Figures 2, 5).

2.

Endemic Tanganyikan G o m p h o c y t h e r e

Gomphocythere species endemic to Lake Tanganyika include G. alata, G. cristata, G. curta, G. lenis, G. simplex, G. n. sp. "coheni", G. n. sp. "downingi", G. n. sp. "'wilsoni" and G. n. sp. "woutersi". Endemic species, as traced over the phylogenetic tree, do not cluster together in a single clade, but instead are interspersed with non-endemics (Figures 5, 6). This indicates that either there were multiple radiations of Gomphocythere species in Lake Tanganyika, or Tanganyikan endemics subsequently dispersed from the lake. The latter possibility is unlikely and would be contrary to the pattern shown by other organisms. Furthermore, G. angulata is known in Late Miocene sediments from northern Kenya. These sediments are only slightly younger than the maximum age for Lake Tanganyika itself (Cohen, 1982) and a Tanganyikan origin for this genus thus appears most improbable. The fact that an endemically constrained tree is not the most parsimonious tree, but has a higher tree length than an unconstrained tree, further supports this conclusion.

Other Lakes

Lake Tenganyika

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Fig. 6. Expected pattern resulting from a single invasion and subsequent radiation of a single species in Lake Tanganyika. 0 ~ 1 indicates character state changes.

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L.E. PARK and K.F. DOWNING

Intralake Distribution

Very little information is available concerning the ostracod faunas of the western (Democratic Republic of Congo) shores of Lake Tanganyika, and most collected material was from the eastern (Tanzania) shore of the lake. However, despite this sampling bias, no species of Gomphocythere was recorded from only one sub-basin or area of the lake.

VI.

DISCUSSION

A. Speciation Model Our speciation model considers two major evolutionary scenarios. The first involves a hypothetical radiation of a "parent" species (p) and five descendant, or "daughter" species (dl-d5) that evolve in a single lake system, taking advantage of the available niche space (nsl-ns6) (Figure 7). Two patterns could result, one with relatively low homoplasy, since each species would evolve to occupy its own niche space, and the species from Lake Tanganyika

S c e n a r i o 1: Sinqle RadiatiOn (with 5 descendant species)

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2. Homoplasy relatively low

Fig. 7. Speciation scenario of a single radiation with five descendant species in a large lake; p, parent species; d, daughter species; ns, niche space. Following such a speciation scenario one would expect to find low levels of homoplasy and autopomorphies that reflect the divergence of the daughter species into well-spaced niches.

OSTRACOD SPECIATION MODES IN LAKE TANGANYIKA

3 17

would nest within their own subclade; or, alternatively, one with higher homoplasy as the populations are isolated and acquire parallel characters independently. This divergence into well-spaced niches would be reflected by the presence of autapomorphies. In contrast, a second scenario involving multiple radiations from two lakes or different sub-basins would reveal a pattern different from that of a single parent and subsequent radiation. Consider the case of six hypothetical species found in one lake, but derived from two different lakes or from different subbasins within a single lake (Figure 8). Lake or lake sub-basin "'A" supports, as before, six individual niche spaces. The daughter species in this lake or subbasin evolve, taking advantage of the most suitable niche spaces available (ns2 ns4). Similarly, in the second lake or lake sub-basin "B", the daughter species also evolve, again taking advantage of the most suitable niche spaces available in that lake oi- sub-basin (ns2 and ns3, where ns2 and as3 are ecologically equivalent in both lakes or sub-basins) (Figure 8). When, for whatever reason, the species of these two lakes or lake sub-basins are brought together, several patterns could emerge, complicating parts of the phylogeny reconstruction, or even making them spurious (Figure 9). One potential pattern is where the dichotomy represents the actual evolution of the sister groups within each lake or lake sub-basin, and reflects actual homoplasy. A second possibility is a pattern resulting from a situation where the number of homoplastic characters overwhelms the phylogenetic sorting role of the true synapomorphies (i.e. autapomorphies playing a role of synapomorphies). This could yield spurious associations of sister groups or, alternatively, imply a type of pseudoreticulation. Because d4 and d5 would evolve in the same approximate niche space as dl and d2, demonstrating parallelism of adaptively derived characters, the patterns emerging from this type of scenario can potentially include high levels of homoplasy (Figure 9). In such a case the autapomorphies would reflect the divergence into well-spaced niches, but similar autapomorphies would be perceived as synapomorphies. Paradoxically, such an example could therefore actually lower homoplasy values for the tree. Which of these two scenarios, single or multiple radiation, is more likely'? Lake Tanganyika has been separated into sub-basins during intervals of low lake-level stand (Tiercelin and Mondeguer, 1991), and this would be consistent with the model if the species within these sub-basins acquired similar character states due to similar environmental parameters. Furthermore, comparison of the favoured phylogeny with the currently known distribution of Gomphocvthere species suggests that the diversity of Gomphocythere in Lake Tanganyika cannot be explained solely in terms of a simple radiation t¥om adjacent lakes. Taken together, these various sources of evidence lead the authors to favour the latter of these two scenarios, one of multiple radiation from adjacent sub-basins of the Tanganyikan trough, as an explanation for the high level of homoplasy seen in the analysis of Gomphocythere in Lake Tanganyika.

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L.E. PARK and K.F. DOWNING

Scenario 2:Multiple Radiations (from 2 lakes or lake sub-basins) (with 5 descendant species) p

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Fig. 8. Speciation scenario of two adjacent lakes or lake sub-basins, A and B, that will subsequently be joined. Lake A has six niche spaces, while B has three. Daughter species dl~13 evolve to occupy niche spaces ns2-ns4 in lake basin A, while in lake B daughter species d4 and d5 evolve to occupy niche spaces ns2 and ns3.

It is also possible that the Gomphocythere lineage was derived from Lake Tanganyika, and then spread outwards via widely dispersed species. This scenario can be tested using fossil evidence to assess the minimum age of any species within this subclade. Gomphocythere angulata has been found in the Late Miocene L o t h a g a m III Formation from Lake Turkana and the Middle to Late Pliocene K o o b i F o r a Formation from east Lake Turkana, showing that its associated branching event must pre-date 7 Mya. Gomphocythereobtusatais also known from the K o o b i Fora Formation of Middle to Late Pliocene age (approximately 2.5 Mya). Neither of these species is present in Lake

OSTRACOD SPECIATION MODES IN LAKE TANGANYIKA

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Scenario 2b: Introduction of "B" species into lake or sub-basin "A"

High homoplasy overall, but not enough to deny true relationships dl and d4 share similar niches and have similar autapomorphies; high homoplasy in "like" habitats (niches) Sister Clusters Dichotomy

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from dl-->d3; dl and d4 falsely represented as sistergroups and d2 and d5 falsely represented as sistergroups; dl and d4 share same niche space, as does d2 and d5

Pattern: 1. Autapomorphies can either be reversed (gained or lost), as in Pattern I; or could become false synapomorphies, forcing the construction of false sister groups. 2. Homoplasy relatively high because d4 and d5 evolve in the same approximate niche space as dl and d2-----> parallelism results

Fig. 9. Speciation scenario of two joined adjacent lakes or lake sub-basins, A and B, and the patterns produced by the overlapping distribution of two similar clades. In the first pattern (upper diagram), the true relationships would be evident, as the tree produced is an unresolved dichotomy. In pattern II, however (lower diagram), dl and d4, and d2 and d5, would be erroneously reconstructed as sister taxa, having similar autapomorphies that are falsely recognized as synapomorphies. This latter pattern could be misconstrued as reticulation (i.e. pseudoreticulation). Thick or normal lines indicate similar autapomorphies; daughter species dl-d3 are from lake basin A, and d4 and d5 are from lake basin B, as indicated in Figure 8. Tanganyika, but both are present in other African lakes, except for Lake Turkana. Lake Tanganyika is estimated to be 9-12 My old (Cohen et al., 1993). The K o o b i F o r a F o r m a t i o n (3.3-2.6 Mya) and L o t h a g a m lIl Formation (4.5-3.5 Mya) are much younger than Tanganyika, and the occurrence of G. angulata and G. obtusata in these formations suggests that these two Gomphocythere species are younger than the formation of Lake Tanganyika. This complicates testing of the Lake Tanganyikan origin hypothesis using these two fossil species. Unfortunately, other than the L o t h a g a m Hill sites, there are few deposits known to be older than Early Pliocene, making further testing of the "Out-of-Tanganyika hypothesis"

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L.E. PARK and K.F. DOWNING

untenable. The minimum age estimate, based on palaeontological evidence for G. angulata and G. obtusata, also suggests that at least parts of the clade could be as old as or older than Lake Tanganyika itself.

B. Speciation in the Tanganyikan Basin Many questions arise in the study of large numbers of closely related taxa occurring within a single lake basin. What is the origin of these faunas? What is their age? When did the ancestors invade the basin? When did the radiation occur? How did these intralacustrine radiations come into existence? Many of the speciation models proposed for species flocks in East African lakes are specific to individual lakes and their basin histories. As such, speciation scenarios in Tanganyika are not necessarily the same as in other ancient lakes. Despite this, the speciation patterns of Gomphocythere (i.e. high homoplasy) in Tanganyika can be compared with other groups that are characterized by morphological divergence and parallel character state acquisitions resulting from multiple radiations. The species assemblages of cichlid fishes in Lakes Victoria, Malawi and Tanganyika have been well studied (Sturmbauer and Meyer, 1992; Meyer, 1993; Lowe-McConnell, 1993; Sturmbauer et al., 1994; Rossiter, 1995; Sultmann et al., 1995; Fryer, 1996; Verheyen et al., 1996; Mayer et al., 1998). The genetic variation within the Tanganyikan cichlid flocks reveals a high degree of within-lake endemism among genetically welt-separated lineages, distributed along the inferred shorelines of three historically intermittent lake basins. The three-clade-three-basin phylogeographical pattern demonstrated by Verheyen et al. (1996) is found twice within the Eretmodini tribe of cichlids. This phylogeographical pattern suggests that major fluctuations in the lake level have been important in shaping the adaptive radiation and speciation within this group. The mitochondrially defined clades are in conflict with the current taxonomy of the group (see Verheyen and Rfiber, this volume) and suggest that there has been convergent evolution in trophic morphology, particularly in the shapes of teeth, taxonomically the most diagnostic character of the three genera. This evolutionary scenario, of multiple radiations from adjacent sub-basins, is similar to that of scenario II in the present model. Evidence presented by the phylogenetic pattern for Gomphocythere suggests it to be the most likely scenario for ostracods in the Tanganyikan trough also. Other authors have also attributed the high amount of genetic diversity within the cichlid fish flocks to geographical isolation due to lake-level fluctuations. For example, in their study of the Tanganyikan genus Tropheus, Sturmbauer and Meyer (1992) propose that, after an initial invasion and radiation, secondary radiations occurred, triggered by fluctuations in lake level. These abiotic factors may have strongly affected the distribution of many

OSTRACOD SPECIATION MODES IN LAKE TANGANYIKA

321

species, and probably led to widespread extinctions and fusions of isolated populations. This, too, is supported by the present phylogenetic analysis of Gomphocythere. Such lake-level fluctuations are likely to have been of great importance, since they have occurred many times in the Tanganyikan trough, and the resultant geographical isolation would potentially have promoted speciation events on each occasion.

C. The Single Invasion Scenario If the diversity of Gomphocythere species observed in Lake Tanganyika were the restllt of a single radiation, then one would expect a single endemic, monophyletic clade within the phylogenetic tree. However, the distribution of non-endemic species within endemic subclades throughout the phylogenetic tree (Figure 5) suggests strongly that there was more than one radiation in the lake and that the Gomphocytherespecies in Lake Tanganyika are not the result of a single radiation. It is probable that some species which arose during these evolutionary bursts became extinct. Evidence lk)r their existence might be uncovered in a longer fossil record, if and when it becomes available.

D. The Multiple Invasion Scenario An immigration scenario explaining the origin of species flocks or clusters requires that dispersal of a sister population from a lake with subsequent reproductive isolation occurs, as well as reintroduction to the lake through immigration. Were this the case, then many of the Gomphocythere species within Lake Tanganyika should have a sister group outside the lake (Smith and Todd, 1984). The presence of some Gomphocytherespecies throughout Africa. and the restriction of others to specific lake systems, could then be explained in terms of multiple invasions. Dispersal of Gompho~Tthere species inhabiting shallow lakes probably takes place via the feet of wading birds. It might also be argued that the wide distribution of Gompho~3"therespecies can be explained by their age alone. If they originated long ago in a single lake or in a series of connected drainages, the presence of Gomphocytherespecies in these various lakes today could be the result of geologically distant isolation and not immigration. However, the presence of Gomphocythereconspecifics in lakes that were never connected in the geological past makes this scenario improbable (Figure 1).

E. Fluctuation in Lake Levels Another hypothesis for species flock formation involves lake-level fluctuations and multiple radiations. Low lake levels would isolate populations into

322

L.E. PARK and K.F. DOWNING

separate water bodies. The different evolutionary pressures (or sufficient time for random mutations) in each water body would mean that each population would be repr6ductively isolated and allopatric speciation would take place. When the lake rose again, the two (or more) newly evolved species would become sympatric. Repeated connection and isolation of basins would provide opportunities for invasions and also for extinctions of species, which would open up possible new niche space for these invading species to occupy. The repeated separation and mixing of species which resulted from lake-level changes in Lake Tanganyika may have promoted species diversity in certain taxa, and has been described as a "species pump" (Rossiter, 1995). There is abundant evidence of lake-level fluctuation in Tanganyika's late Pleistocene history. For example, 50 00(P45 000 years ago and 25 000-15 000 years ago there were low stands of at least 200 m below present water levels. High lake-level stands, 20 m above present levels, occurred between 15 000 and 5000 years ago, when the Kivu basin was open to the Tanganyikan trough (Haberyan and Hecky, 1987; Scholz and Rosendahl, 1988; Tiercelin and Mondeguer, 1991). Lake levels are presently rising, but are 20 m below the maximum lake-level estimates (Jolly et al., 1994). Although a fluctuation in lake levels is an intuitively appealing hypothesis, there is no evidence to support the importance of this mechanism in the evolutionary history of Gomphocythere. For example, one might consider the possibility of vestigial populations, with newly evolved species, separated from each other in subbasins of Lake Tanganyika (i.e. not yet having become sympatric) as circumstantial evidence supporting the fluctuation hypothesis. However, for Gomphocythere, species distributions in Lake Tanganyika are well mixed between sub-basins.

F. Tempo and Mode of GomphocythereSpeciation There is no unequivocal evidence that supports gradualistic or explosive speciation for Gomphocythere in particular, or for ostracods in general, in ancient lakes. Less than 1000 years are represented in the record of cores currently available for Lake Tanganyika and therefore rates of evolution cannot be evaluated by this means. This has led to general evolutionary models of ostracod evolution in these lakes being hypothetical only. For example, Martens (1990) interpreted the contast between the great number of limnocytherid species now present in African lakes and their potential origins within the Holocene as evidence of rapid speciation. He hypothesized that there has been a number of discrete bursts of speciation, interspersed by relatively long periods of stasis. However, there are no geological data to support or refute this idea, and it remains wholly speculative. In fact, evidence suggests that, unlike the haplochromine cichlid fish radiations of Lake Victoria and Lake Malawi (Sturmbauer and Meyer, 1992),

OSTRACOD SPECIATION MODES IN LAKETANGANYIKA

323

the radiation of Gomphocythere occurred early in the lake's history, with little evidence for cladogenesis since the Miocene. Based on current knowledge, it is therefore unrealistic to assume that the diversification of Gomphocythere and other ostracod groups is strictly a Late Pleistocene or Hotocene phenomenon. The presence of non-endemics within Lake Tanganyikan subclades revealed in the present study suggests that the tempo of speciation of Gomphocythere within Lake Tanganyika may have been slow. The data do not support a recent and rapid radiation from a single ancestor. Instead, the topology of the tree suggests that many species are old (pre-Pliocene) and that there have been multiple radiations in the lake. The rate of speciation of the Gomphocythere clade prior to G. angulata remains unknown. Whether the ancestors and their descendants spread over an increasingly large geographical area, with descendant species filling the same or very similar ecological niches in different locations, is not known. However, the distribution pattern resulting from such a situation would be one of a widely distributed ancestor with overlapping ecological distributions, with younger species occupying different ecological niches. It is just such a pattern that the Gomphocythere species show in Lake Tanganyika, where younger taxa show species-specific affinities for different substrates (Park, 1995). VII.

CONCLUSIONS

The analysis suggests that Gomphocythere diversified many times. This interpretation is supported, in part, by the occurrence of non-endemics and endemics in the same subclades. Biogeographical distributions of all Gomphocythere species in Africa indicate that there are no systematic corridors or connected pathways between Gomphocythere faunas in different lakes. In addition, the position of many of the species that occur widely in Africa is at the base of various subclades, suggesting that they might be older than the subclades above them on the tree. Their position, interspersed within, on the Gomphocythere phylogenetic tree also suggests a mosaic pattern of multiple speciation events.

ACKNOWLEDGEMENTS The authors thank A. Cohen, K. Martens, K. Wouters, W. Maddison and D. Maddison for their help in this project. They are also grateful to the reviewers of this manuscript, and especially A. Rossiter for his support and helpfulness. This work was part of L.E. Park's dissertation research at the University of Arizona, and was generously supported by funding from the Geological Society of America, Sigma Xi, Chevron, University of Arizona Analysis of Biological Diversification Research Training Grant and the Sulzer Fund.

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O S T R A C O D S P E C I A T I O N M O D E S IN L A K E T A N G A N Y I K A

Appendix 1: Characters used in cladistic analysis

1. Tubercle 0: absent l: present 2. Venteroposterior flare 0: absent 1: present 3. Surface reticulation 0: reduced l: robust 4. Brood pouch on female 0: absent 1: present 5. Valve shape (dorsal view: anterio>posterior) 0: round 1: oval 2: square 6. Dorsal view o f valve shape 0: convex l: heart 2: triangular 7. Reticulation density of carapace 0: absent 1: < 11 ( p e r 5 # m 2) 2: 12- 17 (per 5 # m 2) 8. Sieve pore 0: normal 1: radial 9. Central muscle scar 0: straight 1: posterior 10. N o d e position 0: absent l: anteroventral 2: posteroventral 3: mediodorsal II. N o d e n u m b e r 0: absent 1:

I

2:

3

12. M a x i m u m dorsal node size 0: absent 1: < 0.1 m m 2: > 0.1 m m 13. M a x i m u m ventral node size 0: absent 1: < 0.1 m m 2: > 0.1 m m 14. Sulcus 0: absent 1: present 15. Alae 0: absent l: present 16. Ventrolateral expansion: alar prolongation 0: absent 1: present 17. O r n a m e n t a l medial ridge 0: absent 1: present 18. Hinge angle 0: parallel 1 : acute 19. Shell thickness 0: thin 1: thick 20. Marginal pore canals 0: < 5/0.1 m m l: > 5,,'0.1 m m 21. Hingement 0: l o p h o d o n t 1: inverse l o p h o d o n t 2: m e r o d o n t 22. Total n u m b e r of furca setae (female) 0: 2 setae each 1: 2 setae and 3 lobes 2: more than 2 setae 23. Distal lobe on hemipenis 0: fixed 1: m o v a b l e

327

328

LE. PARK and K.F. DOWNING

24. Position of furca (male) 0: above copulatory 1: below copulatory 25. Distal lobe apex 0: ridged 1: smooth 26. A1 number of podomeres on endopodite 0:4 1:5 2:6 27. A1 character of 3rd and 4th podomeres 0: separated 1: fused 28. A1 2nd endopodite podomere dorsal apical setae 0: absent 1: present 29. A1 number of claws on the last podomere of endopodite 0: 2 + 2 2: 2 + 1 30. A1 number of mediodorsal setae on 3rd and 4th podomeres 0:

1: 2: 33. A1 1st 0:

35.

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41.

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2 3 position of ventral setae on endopodite absent 1: apically inserted 2: medially inserted

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2: 2 A2 number of podomeres on endopodite 0:3 1:4 A2 1st endopodite podomere apical ventral setae 0: absent 1: present A2 1st endopodite podomere shape 0: rectangular 1: square A2 number of ventral apical setae on 2nd and 3rd podomeres of endopodite 0: 2 1

39. A2 number of mediodorsal setae on 2nd and 3rd podomeres

1

32. A1 number of dorsal apical setae on 3rd and 4th podomeres 0:

1:

1

1: 2 2: 3 31. A1 number of medioventral spines on 3rd and 4th podomeres 0:0 1:

34. A1 number of ventral apical setae on 3rd and 4th podomeres 0: 0

43.

44.

1

1:2 A2 number of medioventral setae on 2nd and 3rd podomeres 0: 3 1:2 2: 1 Mandibular palp 0: bent knee 1: normal Mandibular palp setae 0: bifurcated 1: straight Maxillula palp 0: reduced 1: normal P3 size and shape of terminal claw 0: very elongated 1: slightly elongated and curved 2: short and slightly curved

OSTRACOD SPECIATION MODES IN LAKE TANGANYIKA

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