Peter Holland, homeobox genes, and the developmental basis of animal diversity

In 1867 Alexander Kowalevsky published an account of the development of the cephalochordate Amphioxus lanceolatus (now known as Branchiostoma lanceolatum) (Kowalevsky, 1867). Together with his study of the development of urochordates (Kowalevsky, 1866; 1871), this introduced a new way of thinking about the relationship between the evolution and development of animals, and established the basis for longstanding theories of the evolutionary origin of vertebrates. Some one hundred and fifty years later, cephalochordates and urochordates are again in the spotlight, as molecular biology and genome sequencing promise further revelations about the origin of vertebrates. The work of the 2006 Kowalevsky Medal winner, Peter Holland (Fig. 1), has played a central role in their reinstatement (see Mikhailov and Gilbert (2002) for more details of the history of the Kowalevsky Medal). Here, I profile Peter Holland's contribution to the rebirth of Evolutionary Developmental Biology in general and the study of homeobox genes and vertebrate origins in particular.     

Peter Holland, homeobox genes and the developmental basis of animal diversity

In 1867 Alexander Kowalevsky published an account of the development of the cephalochordate Amphioxus lanceolatus (now known as Branchiostoma lanceolatum) (Kowalevsky, 1867). Together with his study of the development of urochordates (Kowalevsky, 1866; 1871), this introduced a new way of thinking about the relationship between the evolution and development of animals and established the basis for long-standing theories of the evolutionary origin of vertebrates. Some one hundred and fifty years later, cephalochordates and urochordates are again in the spotlight, as molecular biology and genome sequencing promise further revelations about the origin of vertebrates. The work of the 2006 Kowalevsky Medal winner, Peter Holland has played a central role in their reinstatement. Here, I profile Peter Holland's contribution to the rebirth of Evolutionary Developmental Biology in general and the study of homeobox genes and vertebrate origins in particular.     

Discovery of larvae of the hermit crab <Emphasis Type="Italic">Diogenes nitidimanus</Emphasis> Terao, 1913 (Decapoda: Diogenidae) in ship ballast waters: Evidence in support of its introduction into Peter the Great Bay

The larva of the hermit crab Diogenes nitidimanus Terao, 1913 was found in the ballast waters of the tanker Minotaur that arrived from the Chinese port of Laizhou (Bohai Bay, Yellow Sea). Earlier, an abundant population of mature adults of D. nitidimanus was found in Vostok Bay (Peter the Great Bay), this suggested the introduction and naturalization of this species in the Peter the Great Bay. The finding of its larva in ballast waters of a ship on the Russia-China route confirms the introduction of this species into Peter the Great Bay.     

Arenicolous mycelial fungi from the littoral of the Vostok Bay (Peter the Great Bay,the Sea of Japan)

The taxonomic composition of marine mycelial fungi was determined in the interstitial habitats of the Vostok Bay littoral (Peter the Great Bay, the Sea of Japan). A total of 39 species of ascomycetes and anamorphic fungi were detected and identified. The predominant species of the intertidal zone were Corollospora maritima, C. lacera, Carbosphaerella leptosphaerioides, Arenariomyces trifurcatus (Ascomycota), Alternaria alternata, Scolecobasidium arenarium, and Zalerion maritimum (anamorphic fungi). The complete list of species of obligately marine ascomycetes and anamorphic fungi from the interstitial habitats of the Vostok Bay littoral is presented for the first time     

Abundance,distribution, and territory areas of rock-dwelling Lake Tanganyika cichlid fish species

Lake Tanganyika, the second-oldest and second-deepest lake in the world, harbors an impressive cichlid fish fauna counting about 250 endemic species that are characterized by a great level of ecological, morphological, and behavioral specialization. This study describes and compares cichlid fish communities at two rocky shores with differential human impact in the south of Lake Tanganyika. Species inventories and depth-dependent abundances were elaborated. About 41 and 46 sympatric cichlid species were recorded in the two study sites, respectively. Variabilichromis moorii was the most abundant species (29–60% of total number of fishes), followed by Aulonocranus dewindti (3–19%), Tropheus moorii (12%), Ophthalmotilapia ventralis (4–10%), Eretmodus cyanostictus (6–11%), and Cyathopharynx furcifer (0.01–9%). All other species had abundances below 5%. It further emerged that large cichlids such as Petrochromis species, Cyathopharynx furcifer, and Lobochilotes labiatus were very rare at one location, with frequencies of 0.55% or less. Territorial sizes of three particularly abundant species, Variabilichromis moorii, Aulonocranus dewindti, and Tropheus moorii, were assessed by behavioral observations. We distinguished between territorial core areas and total defended area, yielding average core areas between 0.4 (V. moorii) and 1.6 m² (T. moorii), and total defended areas averaging for each species between 1.6 (V. moorii) and 5.0 m² (A. dewindti) with no significant differences between the two study sites. The data on individual densities are also relevant for evolutionary studies, in that they allow more accurate calculations of effective population sizes.     

Flies (Diptera) Associated with <Emphasis Type="Italic">Polygraphus proximus</Emphasis> Blandford, 1894 (Coleoptera,Curculionidae) in Siberia and the Russian Far East

The faunal composition of Diptera (Insecta) inhabiting the galleries of Polygraphus proximus over the territory of Siberia and the Russian Far East was studied. As a result, 14 species of Diptera were discovered representing 8 families. Within its secondary range, the invasive beetle P. proximus Blandford, 1894 is affected not only by the well-known introduced species Medetera penicillata Negrobov, 1970 but also by numerous other widespread predatory flies, such as Medetera excellens Frey, 1909, M. pinicola Kowarz, 1877, Xylophagus cinctus (De Geer, 1776), and Toxoneura ephippium (Zettersted, 1860). Four predatory fly species, M. penicillata, M. signaticornis Loew, 1857, Lonchaea bukowskii Czerny, 1934, and Xylophagus sachalinensis (Pleske, 1925), affect P. proximus within its native range in the Russian Far East. Data on the predation of each species of Diptera on several species of bark beetles testify to their polyphagy. Saprophagous larvae of Dicranomyia modesta (Meigen, 1818), Chalcosyrphus piger (Fabricius, 1794), Xylosciara lignicola (Winnertz, 1867), and Pseudolycoriella unispina (Mohrig et Krivosheina, 1983) were discovered in bark beetle galleries for the first time.     

Autotriploid origin of Carassius auratus as revealed by chromosomal locus analysis

In the Dongting water system, the Carassius auratus (Crucian carp) complex is characterized by the coexistence of diploid forms (2n=100, 2nCC) and polyploid forms. Chromosomal and karyotypic analyses have suggested that the polyploid C. auratus has a triploid (3n=150, 3nCC) and a tetraploid origin (4n=200), respectively. However, there is a lack of direct genetic evidence to support this conclusion. In this paper, analysis of the 5S rDNA chromosomal locus revealed that the 3nCC is of triploid origin. Analysis of the species-specific chromosomal centromere locus revealed that 3nCC individuals possess three sets of C. auratus-derived chromosomes. Our results provide direct cytogenetic evidence suggesting that individuals with 150 chromosomes are of autotriploid origin within the C. auratus complex. It marks an important contribution to the study of polyploidization and the evolution of vertebrates.     

Phylogenetic evidence for an ancestral coevolution between a major clade of coccidian parasites and elasmobranch hosts

Cartilaginous fishes are the oldest jawed vertebrates and are also reported to be the hosts of some of the most basal lineages of Cestoda and Aporocotylidae (Digenea) parasites. Recently a phylogenetic analysis of the coccidia (Apicomplexa) infecting marine vertebrates revealed that the lesser spotted dogfish harbours parasite lineages basal to Eimeria Schneider, 1875 and the group formed by Schellackia Reichenow, 1919, Lankesterella Ames, 1923, Caryospora Leger, 1904 and Isospora Schneider, 1881. In the present study we have found additional lineages of coccidian parasites infecting the cownose ray Rhinoptera bonasus Mitchill and the blue shark Prionace glauca Linnaeus. These lineages were also found as basal to species from the genera Lankesterella, Schellackia, Caryospora and Isospora infecting higher vertebrates. These results confirm previous phylogenetic assessments and suggest that these parasitic lineages first evolved in basal vertebrate hosts (i.e. Chondrichthyes), and that the more derived lineages infect higher vertebrates (e.g. birds and mammals) conforming to the evolution of their hosts. We hypothesise that elasmobranchs might host further ancestral parasite lineages harbouring unknown links of parasite evolution.     

Morphofunctional organization of reserve stem cells providing for asexual and sexual reproduction of invertebrates

Published and original data indicating evolutionary conservation of the morphofunctional organization of reserve stem cells providing for asexual and sexual reproduction of invertebrates are reviewed. Stem cells were studied in representatives of five animal types: archeocytes in sponge Oscarella malakhovi (Porifera), large interstitial cells in colonial hydroid Obelia longissima (Cnidaria), neoblasts in an asexual race of planarian Girardia tigrina (Platyhelmintes), stem cells in colonial rhizocephalans Peltogasterella gracilis, Polyascus polygenea, and Thylacoplethus isaevae (Arthropoda), and colonial ascidian Botryllus tuberatus (Chordata). Stem cells in animals of such diverse taxa feature the presence of germinal granules, are positive for proliferating cell nuclear antigen, demonstrate alkaline phosphatase activity (a marker of embryonic stem cells and primary germ cells in vertebrates), and rhizocephalan stem cells express the vasa-like gene (such genes are expressed in germline cells of different metazoans). The self-renewing pool of stem cells is the cellular basis of the reproductive strategy including sexual and asexual reproduction.     

Polymorphism of <Emphasis Type="Italic">yellow</Emphasis> locus in <Emphasis Type="Italic">Drosophila melanogaster</Emphasis> mutants from natural populations

We have studied the molecular characteristics of the yellow locus (y; 1–0.0), which determines the body color of phenotypically wild-type and mutant alleles isolated in different years from geographically distant populations of Drosophila melanogaster. According to the Southern blot, data restriction maps of the yellow locus of all examined strains differ from one another, as well as from Oregon stock. FISH analysis shows that, in the neighborhood of the yellow locus in the X chromosome, neither P nor hobo elements are found in y^1–775 stock, while only hobo is found in these region in y^1–859 and y^1–866 stocks, only the P element is found in y⁺sn⁸⁴⁹ stock, and both elements are found in y^1–719 stock. Thus, all yellow mutants studied are of independent origin. Locus yellow located on the end of X chromosome (region 1A5–8 on the cytologic map) carries significantly more transposon than retrotransposon induced mutations compared to the white locus (region 3C2). It is possible that, at the ends of Drosophila melanogaster chromosomes, transposons are more active than retrotransposons.     

Adaptations to the hyporheic in Aloninae (Crustacea: Cladocera): allocation of <Emphasis Type="Italic">Alona protzi</Emphasis> Hartwig, 1900 and related species to <Emphasis Type="Italic">Phreatalona</Emphasis> gen. nov.

Morphological study of Alona protzi Hartwig, 1900, Alona phreatica Dumont, 1983 and Alona smirnovi Petkovski &; Flößner, 1972 reveals close affinities with Alona labrosa Vasiljeva &; Smirnov, 1969. We separate these four species from the polyphyletic Alona Baird, 1843 (Anomopoda: Chydoridae). United under Phreatalona gen. nov., these taxa share primitive features on the limbs, together with specializations to a rheic life mode. Phreatalona contains some of the only true hyporheic taxa within the Cladocera. Endemism in two ancient lakes (P. smirnovi and P. labrosa) and a preference for river sediments in Europe (P. phreatica and P. protzi) suggest a long isolation from typical littoral/benthic biotopes. We discuss close links with southern vicariant Nicsmirnovius, the position of these (hypo)rheic chydorids within the subfamily and their affinities with Acroperus. We remark an independent evolution of external (habitus, postabdomen) vs. internal (limb) morphology in the protzi-complex. Phreatalona is likely tertiary in origin, evolving from a littoral alonine adapting to rheic and finally hyporheic environments. Baikal endemic P. labrosa is likely the most primitive species of the genus. We discuss adaptations and evolution in the hyporheic and the effect on dispersal and biogeography of Phreatalona.     

Pistil-function breakdown in a new <Emphasis Type="Italic">S</Emphasis>-allele of European pear, <Emphasis Type="Italic">S</Emphasis><Subscript><Emphasis Type="Italic">21</Emphasis></Subscript>°, confers self-compatibility

European pear exhibits RNase-based gametophytic self-incompatibility controlled by the polymorphic S-locus. S-allele diversity of cultivars has been extensively investigated; however, no mutant alleles conferring self-compatibility have been reported. In this study, two European pear cultivars, ‘Abugo’ and ‘Ceremeño’, were classified as self-compatible after fruit/seed setting and pollen tube growth examination. S-genotyping through S-PCR and sequencing identified a new S-RNase allele in the two cultivars, with identical deduced amino acid sequence as S ₂₁ , but differing at the nucleotide level. Test-pollinations and analysis of descendants suggested that the new allele is a self-compatible pistil-mutated variant of S ₂₁ , so it was named S ₂₁ °. S-genotypes assigned to ‘Abugo’ and ‘Ceremeño’ were S ₁₀ S ₂₁ ° and S ₂₁ °S ₂₅ respectively, of which S ₂₅ is a new functional S-allele of European pear. Reciprocal crosses between cultivars bearing S ₂₁ and S ₂₁ ° indicated that both alleles exhibit the same pollen function; however, cultivars bearing S ₂₁ ° had impaired pistil-S function as they failed to reject either S ₂₁ or S ₂₁ ° pollen. RT-PCR analysis showed absence of S ₂₁ °-RNase gene expression in styles of ‘Abugo’ and ‘Ceremeño’, suggesting a possible origin for S ₂₁ ° pistil dysfunction. Two polymorphisms found within the S-RNase genomic region (a retrotransposon insertion within the intron of S ₂₁ ° and indels at the 3′UTR) might explain the different pattern of expression between S ₂₁ and S ₂₁ °. Evaluation of cultivars with unknown S-genotype identified another cultivar ‘Azucar Verde’ bearing S ₂₁ °, and pollen tube growth examination confirmed self-compatibility for this cultivar as well. This is the first report of a mutated S-allele conferring self-compatibility in European pear.     

A review of the Indo-Pacific bonefishes of the <Emphasis Type="Italic">Albula argentea</Emphasis> complex,with a description of a new species

In this statement about numbers of nominal and valid species, the bonefish Albula argentea (Forster in Bloch and Schneider 1801) of the western and South Pacific, previously regarded as an unavailable name, is a senior synonym of Albula forsteri Valenciennes (an unnecessary replacement name for A. argentea) and A. neoguinaica Valenciennes. It is easily distinguished from the wide-ranging A. glossodonta (Forsskål 1775) by its more pointed lower jaw and higher vertebral and lateral-line scale counts. It is most similar to the Indian Ocean A. oligolepis, described here as a new species, and the endemic Hawaiian A. virgata Jordan and Jordan, resurrected from synonymy. Albula argentea differs from its two related species by higher counts of pored lateral-line scales and vertebrae. It has 68–74 (mode 70) lateral-line scales vs. 61–65 (63) for A. oligolepis and 63–67 (65) for A. virgata, and 71–74 (73) vertebrae vs. 64–66 (65) for A. oligolepis and 65–68 (67) for A. virgata. Albula virgata differs further from A. oligolepis in having the pelvic fin tip reaching beyond the anus (vs. short of or just reaching anus) and higher numbers of scale rows above the lateral line 9–10 (9) vs. 7½–8 (8) for A. oligolepis.     

The effect of environmental conditions on distribution,growth and life span of <Emphasis Type="Italic">Protothaca euglypta</Emphasis> (Mollusca: Bivalvia)

The distribution and growth of the bivalve mollusk Protothaca euglypta in Peter the Great Bay and at the northern boundary of its area were investigated. It is shown that in some biotopes P. euglypta biomass reaches 1–2 kg/m², which exceeds the estimated values of abundance obtained for most associated species of mollusks. It has been established that local variability of P. euglypta growth rates can be compared with latitudinal variability, and the life span increases from the southern part of the area towards its northern boundary. It has been concluded that P. euglypta occupies a more prominent position in the malacofauna of shallow waters in its abundance, than it was considered earlier.