GENETIC AND MORPHOLOGICAL DIVERGENCE AMONG MORPHOTYPES OF THE ISOPOD EXCIROLANA ON THE TWO SIDES OF THE ISTHMUS OF PANAMA

Excirolana braziliensis is a dioecious marine isopod that lives in the high intertidal zone of sandy beaches on both sides of Central and South America. It possesses no larval stage and has only limited means of adult dispersal. Indirect estimates of gene flow have indicated that populations from each beach exchange less than one propagule per generation. Multivariate morphometrics have discovered three morphs of this species in Panama, two of them closely related and found on opposite sides of Central America (“C morph” in the Caribbean and “C′ morph” in the eastern Pacific), the third found predominantly in the eastern Pacific (“P morph”). Though the P and C′ morphs are seldom found on the same beach, they have overlapping latitudinal ranges in the eastern Pacific. A related species, Excirolana chamensis, has been described from the Pacific coast of Panama. Each beach contains populations that remain morphologically and genetically stable, but a single drastic change in both isozymes and morphology has been documented. We studied isozymes and multivariate morphology of 10 populations of E. braziliensis and of one population of E. chamensis. Our objective was to assess the degree of genetic and morphological variation, the correlation of divergence on these two levels of integration, the phylogenetic relationships between morphs, and the possible contributions of low vagility, low gene flow, and occasional extinction and recolonization to the genetic structuring of populations. Genetic distance between the P morph, on one hand, and the other two morphotypes of E. braziliensis, on the other, was as high as the distance between E. braziliensis and E. chamensis. Several lines of evidence agree that E. chamensis and the P morph had diverged from other morphs of E. braziliensis before the rise of the Panama Isthmus separated the C and C′ forms, and that the P morph constitutes a different species. A high degree of genetic differentiation also exists between populations of the same morph. On the isozyme level, every population can be differentiated from every other on the basis of at least one diagnostically different locus, regardless of geographical distance or morphological affiliation. Morphological and genetic distances between populations are highly correlated. However, despite the high degree of local variation, evolution of E. braziliensis as a whole has not been particularly rapid; divergence between the C and C′ morphs isolated for 3 million yr by the Isthmus of Panama is not high by the standard of within-morph differentiation or by comparison with other organisms similarly separated. Alleles that are common in one population may be absent from another of the same morph, yet they appear in a different morph in a separate ocean. The high degree of local differentiation, the exclusive occupation of a beach by one genotype with rare arrival of foreign individuals that cannot interbreed freely with the residents, the genetic stability of populations with infrequent complete replacement by another genetic population, and the sharing by morphs of polymorphisms that are not shared by local populations, all suggest a mode of evolution concentrated in rare episodes of extinction and recolonization, possibly coupled with exceptional events of gene flow that help preserve ancestral variability in both oceans.     

Non-linear loss of suitable wine regions over Europe in response to increasing global warming

Evaluating the potential climatic suitability for premium wine production is crucial for adaptation planning in Europe. While new wine regions may emerge out of the traditional boundaries, most of the present-day renowned winemaking regions may be threatened by climate change. Here, we analyse the future evolution of the geography of wine production over Europe, through the definition of a novel climatic suitability indicator, which is calculated over the projected grapevine phenological phases to account for their possible contractions under global warming. Our approach consists in coupling six different de-biased downscaled climate projections under two different scenarios of global warming with four phenological models for different grapevine varieties. The resulting suitability indicator is based on fuzzy logic and is calculated over three main components measuring (i) the timing of the fruit physiological maturity, (ii) the risk of water stress and (iii) the risk of pests and diseases. The results demonstrate that the level of global warming largely determines the distribution of future wine regions. For a global temperature increase limited to 2°C above the pre-industrial level, the suitable areas over the traditional regions are reduced by about 4%/°C rise, while for higher levels of global warming, the rate of this loss increases up to 17%/°C. This is compensated by a gradual emergence of new wine regions out of the traditional boundaries. Moreover, we show that reallocating better-suited grapevine varieties to warmer conditions may be a viable adaptation measure to cope with the projected suitability loss over the traditional regions. However, the effectiveness of this strategy appears to decrease as the level of global warming increases. Overall, these findings suggest the existence of a safe limit below 2°C of global warming for the European winemaking sector, while adaptation might become far more challenging beyond this threshold.     

Mass mortality of Diadema antillarum on the Caribbean coast of Panama

The ecologically important sea urchin Diadema antillarum suffered mass mortalities in 1983, first noted in Panama and then reported from the rest of the Caribbean. We documented the effects of this mortality at two localities on the Atlantic coast of Panama, Punta Galeta and the San Blas Archipelago. At Punta Galeta, affected by the mortality in January 1983, the numbers of D. antillarum changed from an estimated 14,000 per ha in June 1982 to 0.5 per ha in May 1983; by February 1984 they had increased to 38 per ha. In the San Blas, where mass mortality started in April 1983, the number of D. antillarum in permanent quadrats on 8 reefs was reduced by an average of 94.2%. The average reduction in population density measured in transects on nine reefs was 98.9%. Data taken in permanent quadrats on four reefs in 1978, 1979 and 1980 indicate that population fluctuations of D. antillarum are normally much smaller, justifying the labeling of the 1983 event as mass mortality. Size structure of the San Blas populations was also affected; mean test diameter of D. antillarum on four reefs was reduced from 48.6 mm to 25.0 mm. Other echinoids (Echinometra viridis, E. lucunter, Lytechinus variegatus, L. williamsi, Eucidaris tribuloides, Tripneustes ventricosus, Clypeaster rosaceus and Echinoneus cyclostomus) suffered no ill effects at either Galeta or the San Blas; their population densities remained stable or increased. Density determinations of Diadema mexicanum at the island of Taboguilla on the Pacific side of Panama indicate that Diadema mass mortality did not extend to the eastern Pacific. Sea surface temperatures, tidal levels, rainfall and salinity showed no abnormal fluctuations during the time of D. antillarum mass mortality at Galeta, suggesting that mortality was not due to physical stress. The wide geographical spread and species-specificity of the mortality suggest a water-borne pathogen as the most likely causative agent. Recovery of D. antillarum populations is likely to be slow because there are few, if any, unaffected populations in the Caribbean to contribute larvae for the recolonization of depleted areas. The absence of D. antillarum will probably be reflected by changes in the algal, coral and echinoid communities, and by altered patterns of bioerosion.     

250 million years of bindin evolution

Bindin plays a central role in sperm-egg attachment and fusion in sea urchins (echinoids). Previous studies determined the DNA sequence of bindin in two orders of the class Echinoidea, representing 10% of all echinoid species. We report sequences of mature bindin from five additional genera, representing four new orders, including the distantly related sand dollars, heart urchins, and pencil urchins. The six orders in which bindin is now known include 70% of all echinoids, and indicate that bindin was present in the common ancestor of all extant sea urchins more than 250 million years ago. Over this span of evolutionary time there has been (1). remarkable conservation in the core region of bindin, particularly in a stretch of 29 amino acids that has not changed at all; (2). conservation of a motif of basic amino acids at the cleavage site between preprobindin and mature bindin; (3). more than a twofold change in length of mature bindin; and (4). emergence of high variation in the sequences outside the core, including the insertion of glycine-rich repeats in the bindins of some orders, but not others.     

Phylogeography of the pantropical sea urchin Tripneustes: contrasting patterns of population structure between oceans

To understand how allopatric speciation proceeds, we need information on barriers to gene flow, their antiquity, and their efficacy. For marine organisms with planktonic larvae, much of this information can only be obtained through the determination of divergence between populations. We evaluated the importance of ocean barriers by studying the mitochondrial DNA phylogeography of Tripneustes, a pantropical genus of shallow water sea urchin. A region of cytochrome oxidase I (COI) was sequenced in 187 individuals from locations around the globe. The COI phylogeny agreed with a previously published phylogeny of bindin that barriers important to the evolution of Tripneustes are: (1) the cold water upwelling close to the tip of South Africa, (2) the Isthmus of Panama, (3) the long stretch of deep water separating the eastern from the western Atlantic, and (4) the freshwater plume of the Orinoco and the Amazon rivers between the Caribbean and the coast of Brazil. These barriers have previously been shown to be important in at least a subset of the shallow water marine organisms in which phylogeography has been studied. In contrast, the Eastern Pacific Barrier, 5000 km of deep water between the central and the eastern Pacific that has caused the deepest splits in other genera of sea urchins, is remarkably unimportant as a cause of genetic subdivision in Tripneustes. There is also no discernible subdivision between the Pacific and Indian Ocean populations of this genus. The most common COI haplotype is found in the eastern, central, and western Pacific as well as the Indian Ocean. Morphology, COI, and bindin data agree that T. depressus from the eastern Pacific and T. gratilla from the western Pacific are, in fact, the same species. The distribution of haplotype differences in the Indo-Pacific exhibits characteristics expected from a sea urchin genus with ephemeral local populations, but with high fecundity, dispersal, and growth: there is little phylogenetic structure, and mismatch distributions conform to models of recent population expansion on a nearly global scale. Yet, comparisons between local populations produce large and significant F(ST) values, indicating nonrandom haplotype distribution. This apparent local differentiation is only weakly reflected in regional divergence, and there is no evidence of isolation by distance in correlations between F(ST) values and either geographical or current distance. Thus, Tripneustes in the Indo-Pacific (but not in the Atlantic) seems to be one large metapopulation spanning two oceans and containing chaotic, nonequilibrium local variation, produced by the haphazard arrival of larvae or by unpredictable local extinction.     

Quantitative analysis of gametic incompatibility between closely related species of neotropical sea urchins

Species of the sea urchin genus Echinometra found on the two coasts of Panamá are recently diverged and only partially isolated by incomplete barriers to interspecific fertilization. This study confirms previous work that revealed incompatibility between the eggs of the Atlantic E. lucunter and the sperm of the other two neotropical species, whereas eggs of its sympatric congener E. viridis and allopatric E. vanbrunti are largely compatible with heterospecific sperm. Here we quantify fertilization using a range of sperm dilutions. We demonstrate a much stronger block to cross-species fertilization of E. lucunter eggs than was previously shown at fixed sperm concentrations, and mild incompatibility of the other two species' eggs where previous crosses between species were not distinguishable from within-species controls. Additionally, we present evidence for intraspecific variation in egg receptivity towards heterospecific sperm. Our findings here again discount the "reinforcement model" as a viable explanation for the pattern of prezygotic isolation. Gamete incompatibility in these Echinometra has appeared recently-within the last 1.5 million years-but is weaker in sympatry than in allopatry. Accidents of history may help explain why incompatibility of eggs emerged in one species and not in others. Compensatory sexual selection on sperm in this species could follow, and promote divergence of proteins mediating sperm-egg recognition.     

Echinoids of the Pacific waters of Panama: status of knowledge and new records

This paper is primarily intended as a guide to researchers who wish to know what echinoid species are available in the Bay of Panama and in the Gulf of Chiriqui, how to recognize them, and what has been published about them up to 2004. Fifty seven species of echinoids have been reported in the literature as occurring in the Pacific waters of Panama, of which I have collected and examined 31, including two species, Caenopedina dìomedìae and Meoma frangibilis, that have hitherto only been mentioned in the literature from single type specimens. For the 31 species I was able to examine, I list the localities in which they were found, my impression as to their relative abundance, the characters that distinguish them, and what is known about their biology and evolution. Not surprisingly, most available information concerns abundant shallow water species, while little is known about deep water, rare, or infaunal species.     

POPULATION STRUCTURE AND SPECIATION IN TROPICAL SEAS: GLOBAL PHYLOGEOGRAPHY OF THE SEA URCHIN DIADEMA

Abstract.— The causes of speciation in the sea are rarely obvious, because geographical barriers are not conspicuous and dispersal abilities or marine organisms, particularly those of species with planktonic larvae, are hard to determine. The phylogenetic relations of species in cosmopolitan genera can provide information on the likely mode of their formation. We reconstructed the phylogeny of the pantropical and subtropical sea urchin genus Diadema, using sequences of mitochondrial DNA from 482 individuals collected around the world, to determine the efficacy of barriers to gene flow and to ascertain the history of possible dispersal and vicariance events that led to speciation. We also compared 22 isozyme loci between all described species except D. palmeri. The mitochondrial DNA data show that the two deepest lineages are found in the Indian and West Pacific Oceans. (Indo‐Pacific) Diadema setosum diverged first from all other extant Diadema, probably during the initiation of wide fluctuations in global sea levels in the Miocene. The D. setosum clade then split 3‐5 million years ago into two clades, one found around the Arabian Peninsula and the other in the Indo‐West Pacific. On the lineage leading to the other species of Diadema, the deepest branch is composed of D. palmeri, apparently separated when the climate of New Zealand became colder and other tropical echinoids at these islands went extinct. The next lineage to separate is composed of a currently unrecognized species of Diadema that is found at Japan and the Marshall Islands. Diadema mexicanum in the eastern Pacific separated next, whereas D. paucispinum, D. savignyi, and D. antillarum from the western and central Atlantic, and (as a separate clade) D. antillarum from the eastern Atlantic form a shallow polytomy. Apparently, Indo‐Pacific populations of Diadema maintained genetic contact with Atlantic ones around the southern tip of Africa for some time after the Isthmus of Panama was complete. Diadema paucispinum contains two lineages: D. paucispinum sensu stricto is not limited to Hawaii as previously thought, but extends to Easter Island, Pitcairn, and Okinawa; A second mitochondrial clade of D. paucispinum extends from East Africa and Arabia to the Philippines and New Guinea. A more recent separation between West Indian Ocean and West Pacific populations was detected in D. setosum. Presumably, these genetic discontinuities are the result of water flow restrictions in the straits between northern Australia and Southeast Asia during Pleistocene episodes of low sea level. Diadema savignyi is characterized by high rates of gene flow from Kiribati in the central Pacific all the way to the East African Coast. In the Atlantic, there is a biogeographic barrier between the Caribbean and Brazil, possibly caused by fresh water outflow from the Amazon and the Orinoco Rivers. Diadema antillarum populations of the central Atlantic islands of Ascension and St. Helena are genetically isolated and phylogenetically derived from Brazil. Except for its genetic separation by the mid‐Atlantic barrier, Diadema seems to have maintained connections through potential barriers to dispersal (including the Isthmus of Panama) more recently than did Eucidaris or Echinometra, two other genera of sea urchins in which phylogeography has been studied. Nevertheless, the mtDNA phylogeography of Diadema includes all stages expected from models of allopatric differentiation. There are anciently separated clades that now overlap in their geographic distribution, clades isolated in the periphery of the genus range that have remained in the periphery, clades that may have been isolated in the periphery but have since spread towards the center, closely related clades on either side of an existing barrier, and closely related monophyletic entities on either side of an historical barrier that have crossed the former barrier line, but have not attained genetic equilibrium. Except for D. paucispinum and D. savignyi, in which known hybridization may have lodged mtDNA from one species into the genome of the other, closely related clades are always allopatric, and only distantly related ones overlap geographically. Thus, the phylogenetic history and distribution of extant species of Diadema is by and large consistent with allopatric speciation.     

Demographic history of Diadema antillarum, a keystone herbivore on Caribbean reefs.

The sea urchin Diadema antillarum was the most important herbivore on Caribbean reefs until 1983, when mass mortality reduced its populations by more than 97%. Knowledge of its past demography is essential to reconstruct reef ecology as it was before human impact, which has been implicated as having caused high pre-mortality Diadema abundance. To determine the history of its population size, we sequenced the ATPase 6 and 8 region of mitochondrial DNA from populations in the Caribbean and in the eastern Atlantic (which was not affected by the mass mortality), as well as from the eastern Pacific D. mexicanum. The Caribbean population harbours an order of magnitude more molecular diversity than those of the eastern Pacific or the eastern Atlantic and, despite the recent mass mortality, its DNA sequences bear the genetic signature of a previous population expansion. By estimating mutation rates from divergence between D. antillarum and D. mexicanum, that were separated at a known time by the Isthmus of Panama, and by using estimates of effective population size derived from mismatch distributions and a maximum likelihood coalescence algorithm, we date the expansion as having occurred no more recently than 100 000 years before the present. Thus, Diadema was abundant in the Caribbean long before humans could have affected ecological processes; the genetic data contain no evidence of a recent, anthropogenically caused, population increase.     

Highly contrasted population genetic structures in a host–parasite pair in the Caribbean Sea

Evolution and population genetic structure of marine species across the Caribbean Sea are shaped by two complex factors: the geological history and the present pattern of marine currents. Characterizing and comparing the genetic structures of codistributed species, such as host–parasite associations, allow discriminating the relative importance of environmental factors and life history traits that influenced gene flow and demographic events. Using microsatellite and Cytochrome Oxidase I markers, we investigated if a host–parasite pair (the heart urchin Meoma ventricosa and its parasitic pea crab Dissodactylus primitivus) exhibits comparable population genetic structures in the Caribbean Sea and how the observed patterns match connectivity regions from predictive models and other taxa. Highly contrasting patterns were found: the host showed genetic homogeneity across the whole studied area, whereas the parasite displayed significant differentiation at regional and local scales. The genetic diversity of the parasitic crabs (both in microsatellites and COI) was distributed in two main groups, Panama–Jamaica–St Croix on the one hand, and the South‐Eastern Caribbean on the other. At a smaller geographical scale, Panamanian and Jamaican parasite populations were genetically more similar, while more genetic differentiation was found within the Lesser Antilles. Both species showed a signature of population expansion during the Quaternary. Some results match predictive models or data from previous studies (e.g., the Western‐Eastern dichotomy in the parasite) while others do not (e.g., genetic differentiation within the Lesser Antilles). The sharp dissimilarity of genetic structure of these codistributed species outlines the importance of population expansion events and/or contrasted patterns of gene flow. This might be linked to differences in several life history traits such as fecundity (higher for the host), swimming capacity of larval stages (higher for the parasite), and habitat availability (higher for the host).