Mark V. Erdmann

Biogeography: A marine Wallace's line?

As most coral reef organisms with a pelagic larval phase are presumed to be readily dispersed between distant populations, sea-surface current patterns should be crucial for predicting ecological and genetic connections among threatened reef populations. Here we investigate this idea by examining variations in the genetic structuring of populations of the mantis shrimp Haptosquilla pulchella taken from 11 reef systems in Indonesia, in which a series of 36 protected areas are presumed to be connected by strong ocean currents. Our results reveal instead that there is a strong regional genetic differentiation that mirrors the separation of ocean basins during the Pleistocene low-sea-level stands, indicating that ecological connections are rare across distances as short as 300–400 km and that biogeographic history also influences contemporary connectivity between reef ecosystems.

Sharp genetic breaks among populations of Haptosquilla pulchella (Stomatopoda) indicate limits to larval transport: patterns, causes, and consequences

To help stem the precipitous decline of coral reef ecosystems world‐wide, conservation efforts are focused on establishing interconnected reserve networks to protect threatened populations. Because many coral reef organisms have a planktonic or pelagic larval dispersal phase, it is critical to understand the patterns of ecological connectivity between reserve populations that result from larval dispersal. We used genetics to infer dispersal patterns among 24 Indo‐West Pacific populations of the mantis shrimp, Haptosquilla pulchella. Contrary to predictions of high dispersal facilitated by the strong currents of the Indonesian throughflow, mitochondrial DNA sequences from 393 individuals displayed striking patterns of regional genetic differentiation concordant with ocean basins isolated during periods of lowered sea level. Patterns of genetic structuring indicate that although dispersal within geographical regions with semicontiguous coastlines spanning thousands of kilometres may be common, ecologically meaningful connections can be rare among populations separated by as little as 300 km of open ocean. Strong genetic mosaics in a species with high dispersal potential highlight the utility of genetics for identifying regional patterns of genetic connectivity between marine populations and show that the assumption that ocean currents will provide ecological connectivity among marine populations must be empirically tested in the design of marine reserve networks.

Molecular synapomorphies resolve evolutionary relationships of extant jawed vertebrates

The evolutionary relationships of gnathostomes (jawed vertebrates), which comprise chondrichthyans (cartilaginous fishes), lobe-finned fishes (coelacanths and lungfishes), tetrapods, and actinopterygians (ray-finned fishes), have been debated for almost a century. Phylogenetic analyses based on fossils, morphology, and molecular sequences have generated different models of relationships that remain unresolved. We identified 13 derived shared molecular markers (synapomorphies) that define clades in the vertebrate lineage and used them to resolve the phylogenetic relationships of extant jawed vertebrates. Our markers include the presence or absence of insertions and deletions in coding sequences, nuclear introns, and alternatively spliced transcripts. The synapomorphies identified by us are congruent with each other and give rise to a single phylogenetic tree. This tree confirms that chondrichthyans are basal to all living gnathostomes, that lungfishes (Dipnoi) are the closest living relatives of tetrapods, and that bichirs (Cladistia) are the living members of the most ancient family of ray-finned fishes. Our study also provides molecular evidence to support the monophyly of living tetrapods and teleosts.

COMPARATIVE PHYLOGEOGRAPHY OF THREE CODISTRIBUTED STOMATOPODS: ORIGINS AND TIMING OF REGIONAL LINEAGE DIVERSIFICATION IN THE CORAL TRIANGLE

Abstract The Indonesian‐Australian Archipelago is the center of the worlds marine biodiversity. Although many biogeographers have suggested that this region is a “center of origin,” criticism of this theory has focused on the absence of processes promoting lineage diversification in the center. In this study we compare patterns of phylogeo‐graphic structure and gene flow in three codistributed, ecologically similar Indo‐West Pacific stomatopod (mantis shrimp) species. All three taxa show evidence for limited gene flow across the Maluku Sea with deep genetic breaks between populations from Papua and Northern Indonesia, suggesting that limited water transport across the Maluku Sea may limit larval dispersal and gene flow across this region. All three taxa also show moderate to strong genetic structure between populations from Northern and Southern Indonesia, indicating limited gene flow across the Flores and Java Seas. Despite the similarities in phylogeographic structure, results indicate varied ages of the genetic discontinuities, ranging from the middle Pleistocene to the Pliocene. Concordance of genetic structure across multiple taxa combined with temporal discordance suggests that regional genetic structures have arisen from the action of common physical processes operating over extended time periods. The presence in all three species of both intraspecific genetic structure as well as deeply divergent lineages that likely represent cryptic species suggests that these processes may promote lineage diversification within the Indonesian‐Australian Archipelago, providing a potential mechanism for the center of origin. Efforts to conserve biodiversity in the Coral Triangle should work to preserve both existing biodiversity as well as the processes creating the biodiversity.

Comparative phylogeography of two seastars and their ectosymbionts within the Coral Triangle

Repeated exposure and flooding of the Sunda and Sahul shelves during Pleistocene sea‐level fluctuations is thought to have contributed to the isolation and diversification of sea‐basin populations within the Coral Triangle. This hypothesis has been tested in numerous phylogeographical studies, recovering an assortment of genetic patterns that the authors have generally attributed to differences in larval dispersal capability or adult habitat specificity. This study compares phylogeographical patterns from mitochondrial COI sequences among two co‐distributed seastars that differ in their adult habitat and dispersal ability, and two seastar ectosymbionts that differ in their degree of host specificity. Of these, only the seastar Linckia laevigata displayed a classical pattern of Indian‐Pacific divergence, but with only moderate genetic structure (ΦCT = 0.067). In contrast, the seastar Protoreaster nodosus exhibited strong structure (ΦCT = 0.23) between Teluk Cenderawasih and the remainder of Indonesia, a pattern of regional structure that was echoed in L. laevigata (ΦCT = 0.03) as well as its obligate gastropod parasite Thyca crystallina (ΦCT = 0.04). The generalist commensal shrimp, Periclimenes soror showed little genetic structuring across the Coral Triangle. Despite species‐specific phylogeographical patterns, all four species showed departures from neutrality that are consistent with massive range expansions onto the continental shelves as the sea levels rose, and that date within the Pleistocene epoch. Our results suggest that habitat differences may affect the manner in which species responded to Pleistocene sea‐level fluctuations, shaping contemporary patterns of genetic structure and diversity.

Phylogeography and Limited Genetic Connectivity in the Endangered Boring Giant Clam across the Coral Triangle

The Coral Triangle is the global center of marine biodiversity; however, its coral reefs are critically threatened. Because of the bipartite life history of many marine species with sedentary adults and dispersive pelagic larvae, designing effective marine protected areas requires an understanding of patterns of larval dispersal and connectivity among geographically discrete populations. We used mtDNA sequence data to examine patterns of genetic connectivity in the boring giant clam (Tridacna crocea) in an effort to guide conservation efforts within the Coral Triangle. We collected an approximately 485 base pair fragment of mtDNA cytochrome c oxidase 1 (CO1) from 414 individuals at 26 sites across Indonesia. Genetic structure was strong between regions (phi(ST)=0.549, p < 0.00001) with 3 strongly supported clades: one restricted to western Sumatra, another distributed across central Indonesia, and a third limited to eastern Indonesia and Papua. Even within the single largest clade, small but significant genetic structure was documented (phi(ST)=0.069, p < 0.00001), which indicates limited gene flow within and among phylogeographic regions. Significant patterns of isolation by distance indicated an average dispersal distance of only 25-50 km, which is far below dispersal predictions of 406-708 km derived from estimates of passive dispersal over 10 days via surface currents. The strong regional genetic structure we found indicates potent limits to genetic and demographic connectivity for this species throughout the Coral Triangle and provides a regional context for conservation planning. The recovery of 3 distinct evolutionarily significant units within a well-studied taxonomic group suggests that biodiversity in this region may be significantly underestimated and that Tridacna taxa may be more endangered than currently recognized.

Hox gene clusters in the Indonesian coelacanth, Latimeria menadoensis

The Hox genes encode transcription factors that play a key role in specifying body plans of metazoans. They are organized into clusters that contain up to 13 paralogue group members. The complex morphology of vertebrates has been attributed to the duplication of Hox clusters during vertebrate evolution. In contrast to the single Hox cluster in the amphioxus (Branchiostoma floridae), an invertebrate-chordate, mammals have four clusters containing 39 Hox genes. Ray-finned fishes (Actinopterygii) such as zebrafish and fugu possess more than four Hox clusters. The coelacanth occupies a basal phylogenetic position among lobe-finned fishes (Sarcopterygii), which gave rise to the tetrapod lineage. The lobe fins of sarcopterygians are considered to be the evolutionary precursors of tetrapod limbs. Thus, the characterization of Hox genes in the coelacanth should provide insights into the origin of tetrapod limbs. We have cloned the complete second exon of 33 Hox genes from the Indonesian coelacanth, Latimeria menadoensis, by extensive PCR survey and genome walking. Phylogenetic analysis shows that 32 of these genes have orthologs in the four mammalian HOX clusters, including three genes (HoxA6, D1, and D8) that are absent in ray-finned fishes. The remaining coelacanth gene is an ortholog of hoxc1 found in zebrafish but absent in mammals. Our results suggest that coelacanths have four Hox clusters bearing a gene complement more similar to mammals than to ray-finned fishes, but with an additional gene, HoxC1, which has been lost during the evolution of mammals from lobe-finned fishes.

Tuning of photoreceptor function in three mantis shrimp species that inhabit a range of depths. II. Filter pigments

Abstract. Visual pigments in many animal species, including stomatopod crustaceans, are adapted to the photic environments inhabited by that species. However, some species occupy a diversity of environments as adults (such as a range of depths in the ocean), and a single set of visual pigments would not be equally adaptive for all habitats in which individuals live. We characterized the visual pigment complements of three species of stomatopod crustaceans, Haptosquilla trispinosa, Gonodactylellus affinis, and Gonodactylopsis spongicola, which are unusual for this group in that each lives at depths from the subtidal to several tens of meters. Using microspectrophotometry, we determined the visual pigments in all classes of main rhabdoms in individuals of each species from shallow or deep habitats. Each species expressed the typical diversity of visual pigments commonly found in stomatopods, but there was little or no evidence of differential expression of visual pigments in animals of any species collected from different depths. Vision in these species, therefore, is not tuned to spectral characteristics of the photic environment by varying the assemblages of visual pigments appearing in their retinas.

Reef fishes of the Bird’s Head Peninsula, West Papua, Indonesia

A checklist of shallow (to 60 m depth) reef fishes is provided for the Bird’s Head Peninsula region of West Papua, Indonesia. The area, which occupies the extreme western end of New Guinea, contains the world’s most diverse assemblage of coral reef fishes. The current checklist, which includes both historical records and recent survey results, includes 1,511 species in 451 genera and 111 families. Respective species totals for the three main coral reef areas — Raja Ampat Islands, Fakfak-Kaimana coast, and Cenderawasih Bay — are 1320, 995, and 877. In addition to its extraordinary species diversity, the region exhibits a remarkable level of endemism considering its relatively small area. A total of 26 species in 14 families are currently considered to be confined to the region.

Phylogeography of the crown-of-thorns starfish in the Indian Ocean.

Background Understanding the limits and population dynamics of closely related sibling species in the marine realm is particularly relevant in organisms that require management. The crown-of-thorns starfish Acanthaster planci, recently shown to be a species complex of at least four closely related species, is a coral predator infamous for its outbreaks that have devastated reefs throughout much of its Indo-Pacific distribution. Methodology/Principal Findings In this first Indian Ocean-wide genetic study of a marine organism we investigated the genetic structure and inferred the paleohistory of the two Indian Ocean sister-species of Acanthaster planci using mitochondrial DNA sequence analyses. We suggest that the first of two main diversification events led to the formation of a Southern and Northern Indian Ocean sister-species in the late Pliocene-early Pleistocene. The second led to the formation of two internal clades within each species around the onset of the last interglacial. The subsequent demographic history of the two lineages strongly differed, the Southern Indian Ocean sister-species showing a signature of recent population expansion and hardly any regional structure, whereas the Northern Indian Ocean sister-species apparently maintained a constant size with highly differentiated regional groupings that were asymmetrically connected by gene flow. Conclusions/Significance Past and present surface circulation patterns in conjunction with ocean primary productivity were identified as the processes most likely to have shaped the genetic structure between and within the two Indian Ocean lineages. This knowledge will help to understand the biological or ecological differences of the two sibling species and therefore aid in developing strategies to manage population outbreaks of this coral predator in the Indian Ocean.