Historic dispersal barriers determine genetic structure and connectivity in a supratidal sandy-beach brooder

: The supralittoral zones of sandy beaches are particularly vulnerable to coastal development and other activities that cause localised habitat de-struction. Supratidal species, such as peracarid crustaceans, which lack a pelagic larval phase and tend to avoid direct contact with the swash, are therefore expected to be distributed as isolated populations, with implications for their long-term survival. Genetic population structure of one such species, the pill bug Tylos capensis , was investigated based on mitochondrial cytochrome c oxidase subunit I (COI) haplotype se quences, to assess demographic history and regional population connectivity in the presence of potential dispersal barriers (an estuary, coastal cliffs) along the Indian Ocean coast of South Africa. Here, pill bugs demonstrated strong and significant genetic structure at the regional scale, with 3 distinct clades across the species’ geographic distribution. At a localised spatial scale, coastal cliffs intersecting the high shore appeared to be a strong barrier to gene flow between adjacent populations, while a permanently open estuary did not limit gene flow. Estimates of historic gene flow and patterns of COI differentiation coincided with greater habitat continuity during the Pleistocene glaciations at sea levels between −75 and −120 m, when the African south coast was probably dominated by sandy beaches. While gene flow among low-dispersing pill bug populations is unlikely to benefit from a network of closely spaced coastal protected areas, the isolated nature of this species, coupled with the cryptic diversity inherent in this taxon, emphasizes the need for their protection. The importance of protecting the intact littoral active zone of beaches is highlighted.

[1]  Kyle A. Emery,et al.  Contribution of macroalgal wrack consumers to dissolved inorganic nitrogen concentrations in intertidal pore waters of sandy beaches , 2019, Estuarine, Coastal and Shelf Science.

[2]  S. von der Heyden,et al.  Every beach an island—deep population divergence and possible loss of genetic diversity in Tylos granulatus, a sandy shore isopod , 2019, Marine Ecology Progress Series.

[3]  O. Defeo,et al.  Characterising sandy beaches into major types and states: Implications for ecologists and managers , 2018, Estuarine, Coastal and Shelf Science.

[4]  P. Paiva,et al.  Comparative phylogeography and genetic connectivity of two crustacean species with contrasting life histories on South Atlantic sandy beaches , 2018, Hydrobiologia.

[5]  C. Santamaria,et al.  Molecular approaches uncover cryptic diversity in intertidal Ligia isopods (Crustacea, Isopoda, Ligiidae) across the southern Africa coastline , 2018, PeerJ.

[6]  S. Kojima,et al.  Phylogeography of the sandy beach amphipod Haustorioides japonicus along the Sea of Japan: Paleogeographical signatures of cryptic regional divergences , 2018 .

[7]  C. Duarte,et al.  Light pollution reduces activity, food consumption and growth rates in a sandy beach invertebrate. , 2016, Environmental pollution.

[8]  O. Defeo,et al.  A new evolutionary unit in the Excirolana braziliensis species complex , 2016 .

[9]  Molecular evidence of distinct evolutionary units in the sandhopper Talorchestia capensis (Amphipoda, Talitridae) along South African coasts , 2016, Hydrobiologia.

[10]  K. Gaston,et al.  Quantifying the erosion of natural darkness in the global protected area system , 2015, Conservation biology : the journal of the Society for Conservation Biology.

[11]  C. Matthee,et al.  Genetic isolation by distance reveals restricted dispersal across a range of life histories: implications for biodiversity conservation planning across highly variable marine environments , 2015 .

[12]  K. Yahata,et al.  Phylogeography of Semiterrestrial Isopod, Tylos granuliferus, on East Asian Coasts , 2015, Zoological science.

[13]  J. Dugan,et al.  Local extirpations and regional declines of endemic upper beach invertebrates in southern California , 2014 .

[14]  D. Schoeman,et al.  Rich diversity, strong endemism, but poor protection: addressing the neglect of sandy beach ecosystems in coastal conservation planning , 2014 .

[15]  M. Smale,et al.  Variation in palaeo-shorelines explains contemporary population genetic patterns of rocky shore species , 2014, Biology Letters.

[16]  M. Mateos,et al.  Global Diversification at the Harsh Sea-Land Interface: Mitochondrial Phylogeny of the Supralittoral Isopod Genus Tylos (Tylidae, Oniscidea) , 2014, PloS one.

[17]  O. Pilkey,et al.  Are natural beaches facing extinction? , 2014 .

[18]  M. Beger,et al.  The application of genetics to marine management and conservation: Examples from the Indo-Pacific , 2014 .

[19]  Koichiro Tamura,et al.  MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. , 2013, Molecular biology and evolution.

[20]  M. Mateos,et al.  Contrasting Phylogeography of Sandy vs. Rocky Supralittoral Isopods in the Megadiverse and Geologically Dynamic Gulf of California and Adjacent Areas , 2013, PloS one.

[21]  V. Ketmaier,et al.  Patterns of genetic structuring and levels of differentiation in supralittoral talitrid amphipods: An overview , 2013 .

[22]  P. Haye,et al.  The marine brooder Excirolana braziliensis (Crustacea: Isopoda) is also a complex of cryptic species on the coast of Chile , 2012 .

[23]  O. Defeo,et al.  Coupling between macrofauna community structure and beach type: a deconstructive meta-analysis , 2011 .

[24]  A. von Haeseler,et al.  The performance of phylogenetic algorithms in estimating haplotype genealogies with migration , 2011, Molecular ecology.

[25]  D. Schoeman,et al.  Mapping beach morphodynamics remotely: A novel application tested on South African sandy shores , 2011 .

[26]  J. Compton Pleistocene sea-level fluctuations and human evolution on the southern coastal plain of South Africa , 2011 .

[27]  P. Schembri,et al.  Distribution of Tylos spp. in the Maltese Islands and population dynamics of Tylos europaeus , 2011 .

[28]  M. Hart,et al.  It's about time: divergence, demography, and the evolution of developmental modes in marine invertebrates. , 2010, Integrative and comparative biology.

[29]  C. Peterson,et al.  Give beach ecosystems their day in the sun. , 2010, Science.

[30]  F. Allendorf,et al.  What can genetics tell us about population connectivity? , 2010, Molecular ecology.

[31]  T. Markow,et al.  Mitochondrial DNA evidence for deep genetic divergences in allopatric populations of the rocky intertidal isopod Ligia occidentalis from the eastern Pacific. , 2010, Molecular phylogenetics and evolution.

[32]  L. Excoffier,et al.  Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows , 2010, Molecular ecology resources.

[33]  S. Heyden Why do we need to integrate population genetics into South African marine protected area planning , 2009 .

[34]  P. Beerli,et al.  How to use MIGRATE or why are Markov chain Monte Carlo programs difficult to use , 2009 .

[35]  Julio A. Rozas Liras,et al.  DnaSP v 5 : a software for comprehensive analysis of DNA polymorphism data , 2009 .

[36]  D. Schoeman,et al.  Threats to sandy beach ecosystems: A review , 2009 .

[37]  K. Crandall,et al.  Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified , 2008, Proceedings of the National Academy of Sciences.

[38]  Stephen C. Schroeter,et al.  Ecological effects of coastal armoring on sandy beaches , 2008 .

[39]  C. Duarte,et al.  High Metabolic Rates in Beach Cast Communities , 2007, Ecosystems.

[40]  V. Ketmaier Genetic resources and molecular markers in Talitrus saltator ( Amphipoda , Talitridae ) from the beach of Smir , 2006 .

[41]  F. Jiggins,et al.  Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts , 2005, Proceedings of the Royal Society B: Biological Sciences.

[42]  O. Defeo,et al.  Morphodynamics and habitat safety in sandy beaches: life-history adaptations in a supralittoral amphipod , 2005 .

[43]  M. Pardal,et al.  Biology, population dynamics and secondary production of Tylos europaeus (Isopoda, Tylidae) on the western coast of Portugal , 2005 .

[44]  S. Narum,et al.  Beyond Bonferroni: Less conservative analyses for conservation genetics , 2005, Conservation Genetics.

[45]  Mitchell B Baker,et al.  INCREMENTAL COSTS AND BENEFITS SHAPE NATAL DISPERSAL: THEORY AND EXAMPLE WITH HEMILEPISTUS REAUMURI , 2004 .

[46]  F. Scapini,et al.  Exploratory analysis of talitrid population genetics as an indicator of the quality of sandy beaches , 2003 .

[47]  J. Rozas,et al.  Statistical properties of new neutrality tests against population growth. , 2002, Molecular biology and evolution.

[48]  A. Murray Coastal Geomorphology: An Introduction , 2001 .

[49]  Y. Benjamini,et al.  THE CONTROL OF THE FALSE DISCOVERY RATE IN MULTIPLE TESTING UNDER DEPENDENCY , 2001 .

[50]  Peter Beerli,et al.  Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[51]  P. Schembri,et al.  Patterns of genetic diversity in Mediterranean supralittoral amphipods [Crustacea, Amphipoda] , 2000 .

[52]  L. Scott,et al.  Synthetic reconstructions of southern African environments during the Last Glacial Maximum (21-18kyr) and the Holocene Altithermal (8-6kyr) , 1999 .

[53]  Hawkins,et al.  Extinction risk in the sea. , 1999, Trends in ecology & evolution.

[54]  J. Pechenik On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles , 1999 .

[55]  M. Whitlock,et al.  Indirect measures of gene flow and migration: FST≠1/(4Nm+1) , 1999, Heredity.

[56]  A. C. Brown,et al.  Aggregations of the sandy-beach isopod, Tylos granulatus: adaptation or incidental-effect? , 1999 .

[57]  M. Rex,et al.  Universal cytochrome b primers facilitate intraspecific studies in molluscan taxa. , 1998, Molecular marine biology and biotechnology.

[58]  Y. Fu,et al.  Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. , 1997, Genetics.

[59]  R. Frankham Relationship of genetic variation to population size in wildlife , 1996 .

[60]  S. Carranza,et al.  First molecular evidence for the existence of a Tardigrada + Arthropoda clade. , 1996, Molecular biology and evolution.

[61]  F. Rousset,et al.  AN EXACT TEST FOR POPULATION DIFFERENTIATION , 1995, Evolution; international journal of organic evolution.

[62]  A. Rogers GENETIC EVIDENCE FOR A PLEISTOCENE POPULATION EXPLOSION , 1995, Evolution; international journal of organic evolution.

[63]  R. Vrijenhoek,et al.  DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. , 1994, Molecular marine biology and biotechnology.

[64]  H. Harpending,et al.  Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. , 1994, Human biology.

[65]  A. C. Brown,et al.  The Biology of Oniscid Isopoda of the Genus Tylos , 1994 .

[66]  K. Tamura,et al.  Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. , 1992, Molecular biology and evolution.

[67]  L. Excoffier,et al.  Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. , 1992, Genetics.

[68]  H. Harpending,et al.  Population growth makes waves in the distribution of pairwise genetic differences. , 1992, Molecular biology and evolution.

[69]  M. Slatkin,et al.  Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. , 1991, Genetics.

[70]  A. Mclachlan Ecology of coastal dune fauna , 1991 .

[71]  F. Tajima Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. , 1989, Genetics.

[72]  T. H. Andel Late Pleistocene Sea Levels and the Human Exploitation of the Shore and Shelf of Southern South Africa , 1989 .

[73]  W. Illenberger,et al.  A sand budget for the Alexandria coastal dunefield, South Africa , 1988 .

[74]  B. Kensley Aspects of the biology and ecology of the genus Tylos Latreille , 1970 .

[75]  R. Menzies The Occurrence of a Terrestrial Isopod in Plankton , 1952 .