Damià Jaume

Evolution in caves: Darwin's 'wrecks of ancient life' in the molecular era

Cave animals have historically attracted the attention of evolutionary biologists because of their bizarre ‘regressive’ characters and convergent evolution. However, understanding of their biogeographic and evolutionary history, including mechanisms of speciation, has remained elusive. In the last decade, molecular data have been obtained for subterranean taxa and their surface relatives, which have allowed some of the classical debates on the evolution of cave fauna to be revisited. Here, we review some of the major studies, focusing on the contribution of phylogeography in the following areas: biogeographic history and the relative roles of dispersal and vicariance, colonization history, cryptic species diversity and modes of speciation of cave animals. We further consider the limitations of current research and prospects for the future. Phylogeographic studies have confirmed that cave species are often cryptic, with highly restricted distributions, but have also shown that their divergence and potential speciation may occur despite the presence of gene flow from surface populations. Significantly, phylogeographic studies have provided evidence for speciation and adaptive evolution within the confines of cave environments, questioning the assumption that cave species evolved directly from surface ancestors. Recent technical developments involving ‘next generation’ DNA sequencing and theoretical developments in coalescent and population modelling are likely to revolutionize the field further, particularly in the study of speciation and the genetic basis of adaptation and convergent evolution within subterranean habitats. In summary, phylogeographic studies have provided an unprecedented insight into the evolution of these unique fauna, and the future of the field should be inspiring and data rich.

Making waves: The repeated colonization of fresh water by copepod crustaceans

Twenty-two independent colonizations of fresh and inland continental waters are identified within six of the 10 currently recognized orders of copepods. This number is a minimum estimate and is expected to increase as knowledge of the phylogenetic relationships within copepod families improves. It does not include mere incursions into fresh water, defined as invasions without subsequent diversification (= speciation). The timing of colonization events is estimated, where possible, by inference from biogeographical data. This preliminary analysis supports, in general, a direct relationship between lineage diversity and time elapsed since colonization of fresh water. It is hypothesized that the invasion of South America by the Diaptominae, penetrating from the north, resulted in the displacement of the original calanoid inhabitants of that continent, the Boeckella group within the family Centropagidae, except at high altitude and higher latitudes. A similar, but more ancient, invasion by the Diaptominae is envisaged for Africa, with the original calanoid inhabitants, the Paradiaptominae, now being confined to marginal habitats, such as temporary waters. The analysis indicates a succession of at least four major waves of colonization of inland continental waters, although this may well be an artefact reflecting the indirect method of estimating colonization dates. Taxa currently making incursions into fresh waters may represent the next, or fifth, wave.

Under the volcano: phylogeography and evolution of the cave-dwelling Palmorchestia hypogaea (Amphipoda, Crustacea) at La Palma (Canary Islands).

BackgroundThe amphipod crustacean Palmorchestia hypogaea occurs only in La Palma (Canary Islands) and is one of the few terrestrial amphipods in the world that have adapted to a strictly troglobitic life in volcanic cave habitats. A surface-dwelling closely related species (Palmorchestia epigaea) lives in the humid laurel forest on the same island. Previous studies have suggested that an ancestral littoral Orchestia species colonized the humid forests of La Palma and that subsequent drought episodes in the Canaries reduced the distribution of P. epigaea favouring the colonization of lava tubes through an adaptive shift. This was followed by dispersal via the hypogean crevicular system.ResultsP. hypogaea and P. epigaea did not form reciprocally monophyletic mitochondrial DNA clades. They showed geographically highly structured and genetically divergent populations with current gene flow limited to geographically close surface locations. Coalescence times using Bayesian estimations assuming a non-correlated relaxed clock with a normal prior distribution of the age of La Palma, together with the lack of association of habitat type with ancestral and recent haplotypes, suggest that their adaptation to cave life is relatively ancient.ConclusionThe data gathered here provide evidence for multiple invasions of the volcanic cave systems that have acted as refuges. A re-evaluation of the taxonomic status of the extant species of Palmorchestia is needed, as the division of the two species by habitat and ecology is unnatural. The information obtained here, and that from previous studies on hypogean fauna, shows the importance of factors such as the uncoupling of morphological and genetic evolution, the role of climatic change and regressive evolution as key processes in leading to subterranean biodiversity.

A NEW GENUS OF EPACTERISCID CALANOID COPEPOD FROM AN ANCHIALINE SINKHOLE ON NORTHWESTERN AUSTRALIA

Abstract Bunderia misophaga gen. et sp. nov. is described from an anchialine cenote located on the Cape Range peninsula, northwestern Australia. This is the first epacteriscid calanoid known from Australia and represents the third genus of this family of mainly stygobiont copepods recorded in the Indo-Pacific region. Ordinary phenetic analysis points to the monotypic Enantronoides Fosshagen, Boxshall, and Iliffe, from an anchialine cave on the Bahama Islands, as the closest relative of the new genus. This suggests an ancient, relictual status for the new taxon. The predatory habits of the family Epacteriscidae are confirmed after the gut contents of Bunderia yielded remains of a not-yet-described misophrioid copepod.

Islands beneath islands: phylogeography of a groundwater amphipod crustacean in the Balearic archipelago

BackgroundMetacrangonyctidae (Amphipoda, Crustacea) is an enigmatic continental subterranean water family of marine origin (thalassoid). One of the species in the genus, Metacrangonyx longipes, is endemic to the Balearic islands of Mallorca and Menorca (W Mediterranean). It has been suggested that the origin and distribution of thalassoid crustaceans could be explained by one of two alternative hypotheses: (1) active colonization of inland freshwater aquifers by a marine ancestor, followed by an adaptative shift; or (2) passive colonization by stranding of ancestral marine populations in coastal aquifers during marine regressions. A comparison of phylogenies, phylogeographic patterns and age estimations of clades should discriminate in favour of one of these two proposals.ResultsPhylogenetic relationships within M. longipes based on three mitochondrial DNA (mtDNA) and one nuclear marker revealed five genetically divergent and geographically structured clades. Analyses of cytochrome oxidase subunit 1 (cox1) mtDNA data showed the occurrence of a high geographic population subdivision in both islands, with current gene flow occurring exclusively between sites located in close proximity. Molecular-clock estimations dated the origin of M. longipes previous to about 6 Ma, whereas major cladogenetic events within the species took place between 4.2 and 2.0 Ma.ConclusionsM. longipes displayed a surprisingly old and highly fragmented population structure, with major episodes of cladogenesis within the species roughly correlating with some of the major marine transgression-regression episodes that affected the region during the last 6 Ma. Eustatic changes (vicariant events) -not active range expansion of marine littoral ancestors colonizing desalinated habitats-explain the phylogeographic pattern observed in M. longipes.

The complete mitochondrial genome of the subterranean crustacean Metacrangonyx longipes (Amphipoda): A unique gene order and extremely short control region

Metazoan mitochondrial genomes usually consist of the same gene set, but some taxonomic groups show a considerable variety in gene order and nucleotide composition. The mitochondrial genomes of 37 crustaceans are currently known. Within the malacostracan superorder Peracarida, only three partial mitogenome sequences and the complete sequence of Ligia oceanica (Isopoda) are available. Frequent translocation events have changed the mitochondrial gene order in crustaceans, providing an opportunity to study the patterns and mechanisms of mitogenome rearrangement and to determine their impact on phylogenetic reconstructions. Here we report the first complete nucleotide sequence of an amphipod species, Metacrangonyx longipes, belonging to a phylogenetically enigmatic family occurring in continental subterranean waters. The genome has 14,113 bp and contains the usual 13 protein coding genes and two rRNA subunits, but only 21 out of the typical 22 tRNA genes of Metazoa. This is the shortest mitogenome described thus far for a crustacean and also one of the richest in AT (76.03%). The genome compactness results from a very small control region of 76 bp, the occurrence of frequent gene overlap, and the absence of large non-coding fragments. Six of the protein-coding genes have unusual start codons. Comparison of individual protein coding genes with the sequences known for other crustaceans suggests that nad2, nad6, nad4L and atp8 show the highest divergence rates. M. longipes shows a unique crustacean mitogenome gene order, differing even from the condition found in Parhyale hawaiiensis (Amphipoda), whose coding sequence has also been completed in the present study.

A new genus and two new species of cave-dwelling Misophrioid copepods from the Balearic Islands (Mediterranean)

Speleophriopsis balearicus n. gen., n. sp., and Speleophria gymnesica, n. sp. are described from the flooded coastal karst of the Balearic Is. Two existing species of Speleophria are transferred to the new genus. Speleophriopsis scottodicarloi (Boxshall and Iliffe), new combination, occurs on Bermuda (Atlantic) and S. campaneri (Boxshall and Iliffe), new combination, in the Palau Archipelago (Indo-West Pacific). The type species of Speleophria is known only from caves on Bermuda. Both genera are noteworthy for displaying the most primitive condition known in copepods of the allobasis of maxilla (setal formula 5,3), and of the male antennule which, in Speleophriopsis n. gen., is geniculate but exhibits a 27-segmented condition. They inhabit cave waters with salinities in excess of 18‰., avoiding lower salinity inland groundwater habitats. A Tethyan relict status is proposed for both taxa.

A new species of Exumella (Copepoda: Calanoida: Ridgewayiidae) from anchihaline caves in the Mediterranean

Abstract Exumella mediterranea n. sp., the first representative of the genus outside the Caribbean region, is described. It is a bottom-living inhabitant of anchihaline caves on the Balearic Islands and Sardinia (W Mediterranean). It is a raptorial, opportunistic feeder. Main diagnostic characters separating the new taxon and the other species of the genus are provided by the morphology of the male fifth legs.

Stygocyclopia Balearica, a new genus and species of calanoid copepod (Pseudocyclopiidae) from anchihaline caves in the Balearic Islands (Mediterranean)

Abstract Stygocyclopia balearica, a new genus and species of stygobiont pseudocyclopiid calanoid copepod is described from the Balearic Islands (Mediterranean). It was restricted to anchihaline cave waters with salinities of 18 %0 or more. Its close relationship with Paracyclopia FOSSHAGEN, from anchihaline caves on Bermuda suggests a possible tethyan relict distribution. This is the first record of the family Pseudocyclopiidae SARS in Mediterranean waters.

Two new genera of misophrioid copepods (Crustacea) from an anchihaline cave in the Bahamas

Two new genera of misophrioid copepods are described from an anchihaline cave on the Exuma Cays, Bahamas. Both sexes of Huysia bahamensis are characterized by the retention of biramous fifth legs, a character state previously reported only in members of the Misophria-lineage. Protospeleophria lucayae is described on the basis of a single female. It is closely related to Speleophria, but can easily be distinguished by the more plesiomorphic segmentation pattern of the antennules (the lack of fusion between antennulary segments IX to XII and XV to XVI) and by the maxillipedal armature. The new taxa belong to a cluster of genera, together with Speleophria and Speleophriopsis, characterized by: the presence of a long, falcate rostrum; the fusion between genital and first abdominal somites in the female to form a genital double-somite; the presence of enlarged aesthetascs on antennulary segments III and VII; the [5,3] armature formula of the maxillary allobasis; the 2-segmented endopod of leg 1; and the 4-segm...