Contrasting Phylogeography of Sandy vs. Rocky Supralittoral Isopods in the Megadiverse and Geologically Dynamic Gulf of California and Adjacent Areas

<div><p>Phylogeographic studies of animals with low vagility and restricted to patchy habitats of the supralittoral zone, can uncover unknown diversity and shed light on processes that shaped evolution along a continent’s edge. The Pacific coast between southern California and central Mexico, including the megadiverse Gulf of California, offers a remarkable setting to study biological diversification in the supralittoral. A complex geological history coupled with cyclical fluctuations in temperature and sea level provided ample opportunities for diversification of supralittoral organisms. Indeed, a previous phylogeographic study of <i>Ligia</i>, a supralittoral isopod that has limited dispersal abilities and is restricted to rocky patches, revealed high levels of morphologically cryptic diversity. Herein, we examined phylogeographic patterns of <i>Tylos</i>, another supralittoral isopod with limited dispersal potential, but whose habitat (i.e., sandy shores) appears to be more extensive and connected than that of <i>Ligia</i>. We conducted Maximum Likelihood and Bayesian phylogenetic analyses on mitochondrial and nuclear DNA sequences. These analyses revealed multiple highly divergent lineages with discrete regional distributions, despite the recognition of a single valid species for this region. A traditional species-diagnostic morphological trait distinguished several of these lineages. The phylogeographic patterns of <i>Tylos</i> inside the Gulf of California show a deep and complex history. In contrast, patterns along the Pacific region between southern California and the Baja Peninsula indicate a recent range expansion, probably postglacial and related to changes in sea surface temperature (SST). In general, the phylogeographic patterns of <i>Tylos</i> differed from those of <i>Ligia</i>. Differences in the extension and connectivity of the habitats occupied by <i>Tylos</i> and <i>Ligia</i> may account for the different degrees of population isolation experienced by these two isopods and their contrasting phylogeographic patterns. Identification of divergent lineages of <i>Tylos</i> in the study area is important for conservation, as some populations are threatened by human activities.</p></div

Inferred phylogeny of <i>Tylos</i> in the study area, based on the concatenated mitochondrial+nuclear loci.

<p>Majority-rule consensus tree (RaxML bootstrap). Colors and shapes correspond to clades in Fig. 1. Numbers by nodes indicate the corresponding range of Bootstrap Support (BS; top or left) for Maximum likelihood (RaxML, Garli, PartitionFinder); and Posterior Probabilities (PP; bottom or right) for Bayesian inference methods (MrBayes, Phycas, BayesPhylogenies), including all partitioning schemes. * denotes nodes that received 100% support for all methods. Nodes receiving less than 50% support for all methods were collapsed and denoted with <50. †: relationship based on 16S sequence only: Isla Angel de la Guarda.</p

Sampled localities in the study area.

<p>Colors and shapes correspond to clades in Fig. 2. * denotes location of Guerrero Negro Lagoon in the central Baja California Peninsula.</p

Santamaria_etal_2016_Part2

Santamaria_etal_2016_Part

RaxML bootstrap majority rule consensus tree of the genus <i>Tylos</i>.

<p>Clades with<66% support were collapsed. Based on regular bootstrap partitioned analysis (based on PartitionFinder BIC) of <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094081#pone.0094081.s008" target="_blank">Dataset S2</a> (excluding <i>Helleria brevicornis</i>, which was re-drawn manually). Clade colors correspond to clades in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094081#pone-0094081-g001" target="_blank">Fig. 1</a>. Numbers by nodes indicate the corresponding range of Bootstrap Support and aLRT probabilities (BS; top) for Maximum likelihood (RaxML, Garli, and PhyML); and Posterior Probabilities (PP; bottom) for Bayesian inference methods (MrBayes and Phycas), including all partitioning schemes. * denotes nodes that received 100% support for all methods. ¹Clade support values based on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094081#pone.0094081.s007" target="_blank">Datasets S1</a> analyses (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094081#pone.0094081.s004" target="_blank">Table S3</a>). ²Clade support values based on analyses of dataset excluding <i>H. brevicornis</i>, <i>T. chilensis</i>, <i>T. spinulosus</i>, and <i>T. wegeneri</i> (see text for details). All other support values are based on <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094081#pone.0094081.s008" target="_blank">Dataset S2</a> (see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094081#pone-0094081-t003" target="_blank">Table 3</a>).</p

Description of characters and selected substitution models for Dataset S2 (excluding <i>H. brevicornis</i>).

<p>Description of characters and selected substitution models for <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0094081#pone.0094081.s008" target="_blank">Dataset S2</a> (excluding <i>H. brevicornis</i>).</p

Hawaiian Ligia Data

Includes all morphometrics and molecular data used in the publication

Possible biogeographic scenarios for the three alternative relationships among bythograeid genera.

<p>These scenarios take into account the phylogenetic uncertainty in the <i>GAASC</i> clade for the relationships among <i>Cyanagraea</i>, <i>Segonzacia</i>, and (<i>Allograea</i>+<i>Gandalfus</i>+<i>Austinograea</i>). Bars on nodes depict inferred geographic region shifts if ancestor of Bythograeidae was in the Eastern Pacific (EP; white bars) or in the Mid-Atlantic Ridge (MAR; black bars). Alternative equally parsimonious reconstructions exist in some cases, but are not shown for simplicity. Inferred shifts if ancestor was in Western Pacific (WP) or Central Indian Ridge (CIR) are not depicted, but they would require the largest number of shifts in any of the three topologies.</p

Phylogenetic relationships among members of Bythograeidae based on the concatenated analyses of six genes.

<p>Tree was rooted at the branch joining the two divergent clades (<i>Bythograea</i> and <i>GAASC</i>). Branch lengths are approximate. Bold-faced taxon labels indicate the taxa for which all six genes were obtained and included in the concatenated, species tree, and BCA analyses. The range of support values for concatenated Bayesian, GARLI, and RaxML methods (top to bottom, respectively) are depicted next to the corresponding node (support values for concatenated, species tree, and BCA analyses are shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0032066#pone.0032066.s005" target="_blank">Table S4</a>). Asterisks denote nodes receiving 100% support for all concatenated methods. EP = Eastern Pacific (includes: EPR = Eastern Pacific Rise; GAR = Galapagos Rift; and PAR = Pacific Antarctic Ridge). MAR = Mid-Atlantic Ridge; WP = Western Pacific; CIR = Central Indian Ridge.</p

Bythograeidae samples used in this study.

<p>Bythograeidae samples used in this study.</p