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Impacts of Beach Nourishment on Loggerhead and Green Turtles In A Comparative Study of the Evolution of Multicellularity in the Volvocales Matthew D. Herron and Richard E. Michod Department of Ecology and Evolutionary Biology, University of Arizona Abstract: The volvocine algae (Volvox and its close relatives) represent a Figure 1. Subset of volvocine species: (A) Chlamydomonas Conclusions: unique opportunity for the study of origins of multicellularity. Several major reinhardtii – one undifferentiated • Single origin of coloniality, no evidence of reversal to unicellular cell, (B) Gonium pectorale –a evolutionary transitions have occurred within this relatively young group, clump of 8 undifferentiated cells, condition. which spans a large range of sizes and several levels of complexity. To (C) Eudorina elegans – a spherical colony of 32 undifferentiated cells, • Most recent common ancestor of the Goniaceae and explore the historical and adaptive bases of these major evolutionary (D) Pleodorina californica –a Volvocaceae was likely 16- or 32-celled. transitions, we inferred phylogenetic relationships in the colonial volvocine spherical colony of 32 cells of which a few are terminally • At least four independent origins of large size (>32 cells), with at algae using DNA sequence data. Using maximum parsimony differentiated, (E) Volvox carteri –a spherical colony of up to 4000 least two reductions in cell number. reconstructions of ancestral character states, we traced the evolution of terminally differentiated somatic key innovations such as coloniality, large size, cellular differentiation, and cells and a few specialized • At least three separate origins of germ-soma differentiation reproductive cells, and (F) Volvox novel developmental programs. aureus – a spherical colony of up (partial or complete). to 2000 undifferentiated cells and a • One possible reversal from complete to partial differentiation. few specialized reproductive cells. Origins of multicellularity Photos by C. Solari. • At least two losses of the ancestral developmental program. • Multicellularity has evolved several times independently. Chlamydomonas moewusii (1) Chlamydomonas moewusii Chlamydomonas moewusii Chlamydomonas reinhardtii (1) Chlamydomonas reinhardtii Chlamydomonas reinhardtii • e.g. plants, animals, fungi, red and Chlamydomonas debaryana (1) Chlamydomonas debaryana Chlamydomonas debaryana Vitreochlamys gloeocystiformis (1) Chlamydomonadaceae Vitreochlamys gloeocystiformis Vitreochlamys gloeocystiformis brown algae Vitreochlamys ordinata (1) Vitreochlamys ordinata Vitreochlamys ordinata Vitreochlamys pinguis (1) Vitreochlamys pinguis Vitreochlamys aulata Vitreochlamys pinguis • Complex multicellular organisms Vitreochlamys aulata (1) Basichlamys sacculifera Vitreochlamys aulata Basichlamys sacculifera (4) Tetrabaenaceae Tetrabaena socialis Basichlamys sacculifera Tetrabaena socialis (4) Astrephomene perforata Tetrabaena socialis have functional specialization of cells. Astrephomene perforata (128) 99 Astrephomene gubernaculifera Astrephomene perforata 99 Astrephomene gubernaculifera (128) Gonium pectorale 99 Astrephomene gubernaculifera • Specialization has a cost: some cells Gonium pectorale (16) Gonium octonarium Gonium pectorale Gonium octonarium (8) Gonium quadratum Gonium octonarium Gonium quadratum (16) Goniaceae 80 Gonium multicoccum Gonium quadratum are specialized for functions other than Gonium multicoccum (32) Gonium viridistellatum Gonium multicoccum 80 Gonium viridistellatum (16) Platydorina caudata 80 Volvox globator Gonium viridistellatum reproduction, lowering fecundity. Platydorina caudata (32) Volvox barberi Platydorina caudata Volvox globator (16,000) Volvox rousselettii Volvox globator • This cost, along with multiple Volvox barberi (32,000) Volvulina steinii Volvox barberi Volvox rousselettii (32,000) Volvulina compacta Volvox rousselettii Volvulina steinii (16) 81 Volvulina pringsheimii Volvulina steinii independent origins, suggests that Volvulina compacta (16) Pandorina morum A 60 Volvulina compacta 81 Volvulina pringsheimii (16) Pandorina colemaniae 81 Volvulina pringsheimii multicellularity provides a substantial Pandorina morum A (16) Pandorina morum B Pandorina morum A 60 Pandorina colemaniae (16) 99 Pandorina morum C 60 Pandorina colemaniae benefit. Pandorina morum B (16) Volvulina boldii Pandorina morum B Pandorina morum Yamagishiella unicocca 99 C (16) Eudorina elegans A 99 Pandorina morum C Volvulina boldii (16) Eudorina minodii Volvulina boldii Yamagishiella unicocca (32) Eudorina elegans B Yamagishiella unicocca Volvocine green algae (Volvox and Eudorina elegans A (32) 98 Eudorina unicocca Eudorina elegans A Eudorina minodii (32) Volvox gigas Eudorina minodii its close relatives) are an ideal 1 Eudorina elegans B (32) Volvocaceae Eudorina elegans C Eudorina elegans B 98 Eudorina unicocca (32) 99 Pleodorina indica 98 Eudorina unicocca Volvox gigas (2000) Pleodorina illinoisensis A Volvox gigas system to study origins of 4 85 Eudorina elegans D Eudorina elegans C (32) 1 Eudorina elegans C 8 Pleodorina indica (64) Pleodorina illinoisensis B Pleodorina indica multicellularity. 99 Pleodorina illinoisensis A (32) Eudorina cylindrica 99 Pleodorina californica 2 Pleodorina illinoisensis A 16 85 Eudorina elegans D (32) Pleodorina japonica 85 Eudorina elegans D • More recent origin (35-60 MYA) than Pleodorina illinoisensis B (32) Volvox aureus Pleodorina illinoisensis B 32 Eudorina cylindrica (16) Volvox africanus 3 Eudorina cylindrica Pleodorina californica (128) Volvox dissipatrix Pleodorina californica more complex multicellular groups Pleodorina japonica (128) Volvox tertius 4 Pleodorina japonica >32 Volvox aureus (2000) Volvox obversus Volvox aureus Volvox africanus (8000) Volvox carteri f. nagariensis Volvox africanus • Diverse group with unicellular, Unknown Volvox dissipatrix (16,000) Volvox carteri f. kawasakiensis Unknown Volvox dissipatrix f Volvox tertius (1000) Volvox carteri .weismannia Volvox tertius multicellular, and several intermediate Volvox obversus (2000) 5% Volvox obversus Volvox carteri f. nagariensis (4000) 5% Volvox carteri f. nagariensis stages 5% Volvox carteri f. kawasakiensis (2000) Volvox carteri f. kawasakiensis Volvox carteri f.weismannia (2000) Volvox carteri f.weismannia GS: Undifferentiated cells (Germ-Soma) • Easily cultured, rapid generations GS/S: Undifferentiated cells (GS) and somatic cells (S) (1) G/S: Separate germ cells and somatic cells Figure 4. Four developmental programs mapped onto the Bayesian phylogeny: (1), • Well-studied ecology, cytology, Unknown gonidia (reproductive cells) grow large and divide rapidly without further growth to genetics, development Figure 2. Numbers of cells mapped onto the Bayesian phylogeny. At least four separate produce equal-sized daughter cells; (2), an early asymmetric division creates large cells origins of large size (>32 cells) are evident. Gonium octonarium and Eudorina cylindrica Figure 3. Three levels of germ-soma differentiation mapped onto the Bayesian that develop into gonidia; (3), similar to (1) but divisions are slow; (4), gonidia are small • Possible multiple origins of represent probable reductions in cell number. phylogeny. At least three separate origins of partial or complete functional and grow between cell divisions, which are symmetrical. At least two independent losses specialization of cells are evident. Pleodorina californica and P. japonica may represent of the ancestral developmental program (program 1) are evident. characters related to multicellularity a reversal from G/S to GS/S. Major evolutionary transitions in the volvocine algae: Methods: References: • From unicellular to colonial • DNA sequences from five chloroplast genes (atpB, psaA, psaB, psbC, rbcL) 1. A. G. Desnitski, Eur. J. Protistol. 31, 241 (1995). 2. D. Posada, K. Crandall, Bioinformatics 14, 817 (1998). • From simple clumps of cells to structured hollow spheres combined into a supermatrix 3. F. Ronquist, J. P. Huelsenbeck, Bioinformatics 19, 1572 (2003). • From undifferentiated cells to partial specialization • Best-fit model of nucleotide substitution inferred in Modeltest(2) 4. W. P. Maddison, D. R. Maddison. http://mesquiteproject.org (2004). • From partial specialization to complete separation of reproductive and • Phylogeny inferred using Bayesian methods in MrBayes(3) somatic functions Acknowledgements: • Posterior probabilities calculated from 3.0 x 106 post-burnin generations We thank C. Solari for providing photographs and helpful advice, M. • Among sizes that span five orders of magnitude • Ancestral character states inferred using maximum parsimony in Mesquite(4) Buchheim for generously providing unpublished DNA sequences, •In Volvox, among four distinct developmental programs(1) and A. Coleman and H. Nozaki for helpful advice..
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