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Graeme T. Lloyd <Graeme.Lloyd@Bristol.Ac.Uk> Can palaeobiogeography explain low rates of morphological evolution in ‘living fossil’ lungfish? Graeme T. Lloyd <[email protected]> n=124 Introduction Methods and Materials A B In a classic work Westoll (1949) used a character-taxon matrix to show that Aside from the inevitable addition of new taxa and refinements to the lungfish underwent rapid morphological evolution early in their history geological timescale since 1949 there are some significant flaws in No followed by an extended period of morphological stagnation (Figure 1): a Westoll’s method: 1) the ancestor is purely hypothetical, 2) a selective Change textbook example (literally) of evolution in a ‘living fossil’. Here I update suite of taxa was used, 3) error bars (missing data) constrain Contraction 45 Westoll’s method for use with cladistic datasets and place it in its correct interpretation, 4) a stratigraphically ordered ancestor-descendant 55.5 phylogenetic context. One proposed explanation for the existence of living sequence was assumed, and 5) reversal (character loss) wasn’t taken into fossils is geographic isolation in refugia, where lack of competition negates account. Although modern cladistic matrices are more inclusive and more Expansion the need for morphological change. Here this hypothesis is tested by often contain a real outgroup (answering points 1 and 2 above) missing 23.5 C comparing lungfish dispersal patterns during their rapid Devonian phase data is still a major issue. To overcome this the internal nodes (rather than with their slower post-Devonian phase of evolution. the taxa themselves) were scored as these are complete under a given phylogenetic hypothesis. Nodes were scored as the total number of Figure 4 The Devonian (rapid phase) of lungfish evolution (416 - 385.3Ma). A a palaeogeo- accumulated character changes between that node and the root. Here graphic map of the Early Devonian (source: www.scotese.com). B a pie-chart showing the relative proportion of branches that reflect range expansion, contraction or continuity (no DELTRAN was used as it dumps equivocal changes on the terminal change). C The long-snouted marine genus Griphognathus known from the Late Devonian branches (which aren’t used). Nodes were dated based on the stage of Europe and Australia. A B mid-point (using Gradstein et al., 2004) of the oldest taxon stemming from it. Here this method is applied to a ‘supermatrix’ (of 86 taxa and 132 morphological characters) based on six published cladistic analyses of lungfish interrrelationships. A B n=46 Palaeobiogeographic analysis involved assignment of each taxon to a geographic region, in this case modern continents. Despite lungfish No undergoing a change in habitat preference from marine to freshwater Change environments it is assumed that this didn’t significantly affect dispersal Contraction 16 patterns, especially as Mesozoic taxa are thought to have retained a 19.5 C tolerance to marine conditions (Schultze 2004). Ancestral distributions were then reconstructed using Fitch (1972) parsimony. Each branch was Expansion then classified as either: a) a range expansion (e.g. a change from an 10.5 Australasian distribution to an Australasian plus Asian distribution), b) a range contraction (e.g. a Eurasian distribution to an Asian distribution) or, Figure 1 A classic work in macroevolution. A Thomas Stanley Westoll (1912 - 1995) B The results of c) no change. Figure 5 The post-Devonian (slow phase) of lungfish evolution (385.3Ma - Pres- Westoll’s study of the evolution of the lungfish character complex. Sixteen dipnoan taxa (A - M) were ent). A a palaeogeographic map of the Permian (source: www.scotese.com). B a scored from 100 (primitive ancestor) to 0 (the extant Lepidosiren and Protopterus). The slope of the graph pie-chart showing the relative proportion of branches that reflect range expan- represents the rate of evolution, with the steep rapid phase contained within the Devonian. sion, contraction or continuity (no change). C The extant species Protopterus an- nectens known from modern day Africa. $EVONIAN POST $EVONIAN RAPIDPHASE SLOWPHASE !CCUMULATEDCHARACTERCHANGES Psarolepis [AS] Discussion AS Diabolepis [AS] Westollrhynchus [EU] The broad congruence between the results presented here and those of Westoll suggest either that the pattern AS,AU,EU Ichnomylax [AU] AU Chirodipterus onawayensis [NA] AU,EU AU,NA Dipnorhynchus cathlesae [AU] of two evolutionary tempos for lungfish is robust, and hence biologically real, or consistently biased, either by AU Dipnorhynchus kiandrensis [AU] Archaeonectes [EU] AU worker methodology or the fossil record. A more comprehensive discussion of the causes of this disparity is AU,EU Speonesydrion iani [AU] AU Dipnorhynchus sussmilchi [AU] AU Dipnorhynchus kurikae [AU] given elsewhere (Lloyd, in prep.). However, the results presented here present strong evidence that AU,EU,NA AU,EU Jessenia [EU] Uranolophus [NA] palaeobiogeographic processes do not impact on rates of lungfish evolution at all. Interestingly lungfish seem to Melanognathus [NA] NA Stomiahykus [NA] NA Tarachomylax [AS] show no retardation of dispersal ability following their transition from marine to freshwater environments, EU,NA AS,EU Dipterus valenciennesi [EU] Dipterus cf. valenciennesi [EU] EU although it seems likely that dispersal rates did drop off as the branches used in the post-Devonian phase Adalolopas [AU] AU,EU Adelargo [AU] represent larger spans of time. The three extant genera (Lepidosiren, Neoceratodus and Protopterus) are more AU AU Barwickia [AU] AU,EU Chirodipterus rhenanus [EU] Chirodipterus wildungensis [EU] AU closely related to each other than almost all of the extinct taxa and are now restricted to freshwater habitats in Chirodipterus australis [AU] AU,EU,NA Pillarhynchus [AU] AU,EU RAPIDPHASE Sorbitorhynchus [AS] the southern hemisphere (South America, Australia and Africa respectively). It seems probable that this shift AS,NA Iowadipterus [NA] $EVONIAN AS,AU,EU,NA AU Palaedaphus [EU,AS] towards a more endemic distribution, and the last intercontinental dispersal, didn’t occur until the Cretaceous AS Orlovichthys [AS] AS,NA Sunwapta [NA] AU,EU Rhinodipterus ulrichi [EU] period, some 200 million years after evolutionary rates dropped off dramatically. EU Rhinodipterus secans [EU] AS,EU Rhinodipterus stolbovi [AS] Eoctenodus [AU] 4IME-A AU,EU Gogodipterus [AU] AU,EU Grossipterus crassus [EU] Figure 3 The results of the application of the cladistic modification of Westoll’s (1949) original method. AU,EU Holodipterus santacrucensis [EU] AU Holodipterus elderae [AU] AU,EU Note the broad congruence with Westoll’s original results and the split between the two tempos of lungfish AU Holodipterus gogoensis [AU] AU Holodipterus longi [AU] evolution. (Open circles indicate freshwater habits and closed circles marine habits; grey lines describe Acknowledgements AU Holodipterus meemannae [AU] AU,EU the branching structure of the phylogeny in Figure 2). Howidipterus [AU] This work is part of my PhD project which was initially conceived by Oervigia [EU] Andreyevichthys [AS] EU Fleurantia [NA] my supervisors, Phil Donoghue and Mike Benton (both University of AU,EU AS,EU,NA Jarvikia [EU] EU,NA EU Soederberghia groenlandica [EU] Bristol) and is funded by a NERC studentship. Hans-Peter Schultze AU,EU Soederberghia simpsoni [AU] EU Rhynchodipterus [EU] EU EU Griphognathus minutidens [EU] Results (University of Kansas) kindly provided me with a copy of his unpub- EU Griphognathus sculpta [EU] AU,EU Griphognathus whitei [AU] A phylogenetic tree was derived from the ‘supermatrix’ (based first on parsi- lished lungfish matrix and Matt Friedman (University of Chicago) Phaneropleuron [EU] Delatitia [AU] EU Pentlandia [EU] mony analysis and then on stratigraphic ‘fit’) and ancestral distributions shared useful advice concerning the finer points of lungfish tax- AU,EU EU,NA Scaumenacia [NA] Straitonia [EU] added (Figure 2). Despite the various modifications made here the results for onomy. Leonard P. Annectens (Departmental Lungfish, University of EU EU,NA Tranodis [NA] Ctenodus [EU] EU Ganopristodus [EU] lungfish (Figure 3) are broadly congruent with Westoll’s original analysis Bristol: at right) is thanked for his contributions to my knowledge of EU EU Nielsenia [EU] EU Conchopoma [NA,EU] (Figure 1; note Westoll’s graph can be considered as ‘upside-down’ as he lungfish anatomy. Sandra Jasinoski and Sarda Sahney (both Uni- EU,NA Sagenodus [NA,EU] Palaeophichthys [NA] NA Megapleuron [NA,EU] was investigating a loss of primtive characters whereas here the focus is on versity of Bristol) gave useful advice on an earlier draft of this NA Paraceratodus [AF] Gosfordia [AU] POST $EVONIAN acquired characters). Using this data the tree was split into two parts ref- poster. Outstanding errors, the garish colour scheme and overuse AF,AS,EU,NA AU Archaeoceratodus [AU] AU Asiatoceratodus [AS] SLOWPHASE Neoceratodus [AU] electing the two evolutionary ‘tempos’ (a rapid Devonian phase and a much AF,AU AS,AU of drop shadows are solely attributable to the author. AU Mioceratodus [AU] AF,AU,SA Lepidosiren [SA] slower post-Devonian phase). The results here (Figures 4B and 5B) show AF,SA Protopterus [AF] AU Microceratodus [AF] Namatozodia [AU] that the slower phase actually reflects an increase in range expansion at the AF,AU AU Ariguna [AU] Figure 2 The phylogeny of lungfish used AF,AS,AU Beltanodus [AF] expense of both range contraction or continuity of range. However, a chi- AF,AS Parasagenodus [AS] here. Terminal taxa and internal nodes are AU AS Gnathoriza [NA,AS] References cited Ptychoceratodus [AF,AS,AU,EU] squared test shows that there is no significant difference (p 0.99-0.975) be- assigned to continents (AF = Africa, AS = AU Aphelodus [AU] FITCH, W. M., 1971. Towards defining the course of evolution: minimum change for a specific tree topology. Systematic Zoology, 20, 406-416. Ceratodus sturii [EU] AU tween the relative proportions of expansion, contraction and continutiy be- GRADSTEIN, F. M., J. G. OGG and A. G. SMITH, 2004. A Geologic Time Scale 2004. Cambridge University Press, Cambridge. Asia, AU = Australasia, EU = Europe, NA EU Ceratodus latissimus [EU] AS,AU,EU Ferganoceratodus [AS] SCHULTZE, H.-P., 2004.
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