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.     

Origin and early evolution of the vertebrates: new insights from advances in molecular biology, anatomy, and palaeontology

Recent advances in molecular biology and microanatomy have supported homologies of body parts between vertebrates and extant invertebrate chordates, thus providing insights into the body plan of the proximate ancestor of the vertebrates. For example, this ancestor probably had a relatively complex brain and a precursor of definitive neural crest. Additional insights into early vertebrate evolution have come from recent discoveries of Lower Cambrian soft body fossils of Haikouichthys and Myllokunmingia (almost certainly vertebrates, possibly related to modern lampreys) and Yunnanozoon and Haikouella (evidently stem-group vertebrates). The earliest vertebrates had an unequivocally marine origin, probably evolved mineralised pharyngeal denticles before the dermal skeleton, and evidently utilised elastic recoil of the visceral arch skeleton for suction feeding. Moreover, the new data emphasise that the advent of definitive neural crest was supremely important for the evolutionary origin of the vertebrates.     

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 (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.     

文昌鱼特异的基因倍增

进化生物学和发育生物学的结合产生了一门新兴学科——进化发育生物学,近年来该领域研究取得了丰硕的成果。头索动物文昌鱼是现存生物中最近似于脊椎动物直接祖先的生物,在与脊椎动物分化后形态改变很小,其基因组未曾经历大规模的基因组倍增,在一定程度上反映了脊椎动物祖先型基因组的特征,但在漫长的独立进化历程中基因组自身还是经历了一些变化。本文介绍了在几例在文昌鱼支系中独立发生的基因倍增事件(Hox; Evx; HNF-3; Calmodulin-like),有力地揭示了文昌鱼虽然与脊椎动物直接祖先极其接近,但其基因组有其自身特性,不能简单地将之等同于脊椎动物直接祖先。Abstract: The union of the two complementary disciplines, developmental biology and evolutionary biology resulted in a new division of evolutionary developmental biology, namely “Evo-Devo”. Recently, the research on this field has been fruitful in understanding the origin and development of vertebrates. The cephalochordate amphioxus, which remains in relatively invariant morphology since the divergence from the vertebrate lineage, is the closest living relative to vertebrates. The vertebrate-like simple body plan and preduplicative genome provide amphioxus genes the privilege to serve as key landmark to understand morphological evolution. However, the amphioxus genome has not escaped evolution. In this paper several examples of independent gene (Hox; Evx; HNF-3 and Calmodulin-like) duplications in the cephalochordate lineage were summarized. These particularities and oddities remind the fact that amphioxus is not an immediate ancestor of the vertebrates but ‘only’ the closest living relative to the ancestor, with a mix of prototypical and amphioxus-specific features in its genome.     

A celebration of the new head and an evaluation of the new mouth

Twenty years ago now, Carl Gans and Glen Northcutt proposed that the main invention of vertebrates was a new head, with its full array of sensory organs involved in an active predatory lifestyle. Tracing back the embryological origin of these structures, they showed how all are primarily derived from the neural crest and the placodes, two transient ectodermal cell populations in the embryo. These cell types were then used for further innovations, such as a new mouth in jawed vertebrates. The interplay between patterning and plasticity of the neural crest is largely responsible for the endless variation of vertebrate craniofacial features in evolution.     

Mites of the family Cheyletidae (Acari: Prostigmata): phylogeny, distribution, evolution and analysis of parasite-host relationship

A modern system, phylogeny, distribution and host parasite relationships of cheyletid mites (Acari: Prostigmatal Cheyletidae) is shortly discussed. According to the phylogenetic hypothesis proposed by Bochkov and Fain (2001), the family Cheyletidae includes now 15 tribes: Acaropsellini, Bakini, Cheletogenini, Cheletosomatini, Chelonotini, Cheyletiini, Cheyletiellini, Cheyletini, Cheletomorphini, Criokerontini, Metacheyletiini, Niheliini, Ornithocheyletiini, Teinocheylini and one unnamed tribe including the genera Caudacheles and Alliea. The parasitic Cheyletidae were primarily free-living predators, frequently associated with nests of vertebrates. These mites, being predators, have numerous preadaptations to the parasitic mode of life and they possess high ecological plasticity. Therefore it was quite easy for these mites to adapt to parasitism on the vertebrates. According to our phylogenetical hypothesis, the parasitism on vertebrates has arisen independently in several phylogenetic lines of the cheyletids associated with nests of vertebrates. Such transition from nest predation to true parasitism probably occurred repeatedly and at different times. The cheyletid mites are more widely represented on birds than on mammals. Possibly, it is in relation with a more early origin of parasitism in the cheyletids associated with bird nests than in the cheyletids associated with mammal nests. An independent origin of the parasitism in many different cheyletid phyletic lines, arisen significantly later than the origin of such a parasitic group as myobiid mites, is probably the main reason, which could explain the recent mosaic distribution of the Cheyletidae among the mammalian taxa. Parasitic associations between cheyletids and vertebrates are more common than the associations between these mites and the invertebrates. In the invertebrates, these associations are generally restricted to a phoresy. The zoogeographical analysis showed that this family as whole is characterised by the extremely low endemisms. The most part of the free-living cheyletid mites are associated with Holarctic region (87%) and, therefore, this family, probably, originated there.     

The new head hypothesis revisited

In 1983, a new theory, the New Head Hypothesis, was generated within the context of the Tunicate Hypothesis of deuterostome evolution. The New Head Hypothesis comprised four claims: (1) neural crest, neurogenic placodes, and muscularized hypomere are unique to vertebrates, (2) the structures derived from these tissues allowed a shift from filter feeding to active predation, (3) the rostral head of vertebrates is a neomorphic unit, and (4) neural crest and neurogenic placodes evolved from the epidermal nerve plexus of ancestral deuterostomes. These claims are re-examined within the context of evolutionary developmental biology. The first may or may not be valid, depending on whether protochordates have these tissues in rudimentary form. Regarding the second, clearly, the elaboration of these tissues in vertebrates is correlated with a shift from filter feeding to active predation. The third claim is clarified, i.e., that the elaboration of the alar portion of the rostral brain and the development of olfactory organs and their associated connective tissues represent a neomorphic unit, which appears to be valid. The fourth is rejected. When the origin of neural crest and neurogenic placodes is examined within the context of developmental biology, it appears they evolved due to the rearrangement of germ layers in the blastulae of the deuterostomes that gave rise to chordates. Deuterostome evolution and the origin of vertebrates are also re-examined in the context of new data from developmental biology and taxonomy. The Tunicate Hypothesis is rejected, and a new version of the Dipleurula Hypothesis is presented.     

Windows of the brain: towards a developmental biology of circumventricular and other neurohemal organs

We review the anatomical and functional features of circumventricular organs in vertebrates and their homologous neurohemal organs in invertebrates. Focusing on cyclostomes (lamprey) and urochordates (ascidians), we discuss the evolutionary origin of these organs as a function of their cell type specification and morphogenesis.     

Amphioxus type I keratin cDNA and the evolution of intermediate filament genes.

We report the cloning of an intermediate filament (IF) cDNA from the cephalochordate amphioxus that encodes a protein assignable to the type I keratin group. This is the first type I keratin reported from an invertebrate. Molecular phylogenetic analyses reveal that amphioxus also possesses a type II keratin, and that the genes encoding short-rod IF proteins underwent different patterns of duplication in vertebrates and their closest relatives, the cephalochordates. Extensive IF gene duplication and divergence may have facilitated the origin of new specialised cell types in vertebrates.     

Amphioxus and tunicates as evolutionary model systems

One important question in evolutionary biology concerns the origin of vertebrates from invertebrates. The current consensus is that the proximate ancestor of vertebrates was an invertebrate chordate. Today, the invertebrate chordates comprise cephalochordates (amphioxus) and tunicates (each a subphylum in the phylum Chordata, which also includes the vertebrate subphylum). It was widely accepted that, within the chordates, tunicates represent the sister group of a clade of cephalochordates plus vertebrates. However, recent studies suggest that the evolutionary positions of tunicates and cephalochordates should be reversed, the implications of which are considered here. We also review the two major groups of invertebrate chordates and compare relative advantages (and disadvantages) of each as model systems for elucidating the origin of the vertebrates.     

It's a long way from amphioxus: descendants of the earliest chordate

The origin of chordates and the consequent genesis of vertebrates were major events in natural history. The amphioxus (lancelet) is now recognised as the closest extant relative to the stem chordate and is the only living invertebrate that retains a vertebrate‐like development and body plan through its lifespan, despite more than 500 million years of independent evolution from the stem vertebrate. The inspiring data coming from its recently sequenced genome confirms that amphioxus has a prototypical chordate genome with respect to gene content and structure, and even chromosomal organisation. Pushed by joint efforts of amphioxus researchers, amphioxus is now entering a new era, namely its maturation as a laboratory model, through the availability of a large amount of molecular data and the advent of experimental manipulation of the embryo. These two facts may well serve to illuminate the hidden secrets of the genetic changes that generated, among other vertebrates, ourselves.     

An evolutionary perspective on the systems of adaptive immunity

We propose an evolutionary perspective to classify and characterize the diverse systems of adaptive immunity that have been discovered across all major domains of life. We put forward a new function‐based classification according to the way information is acquired by the immune systems: Darwinian immunity (currently known from, but not necessarily limited to, vertebrates) relies on the Darwinian process of clonal selection to ‘learn’ by cumulative trial‐and‐error feedback; Lamarckian immunity uses templated targeting (guided adaptation) to internalize heritable information on potential threats; finally, shotgun immunity operates through somatic mechanisms of variable targeting without feedback. We argue that the origin of Darwinian (but not Lamarckian or shotgun) immunity represents a radical innovation in the evolution of individuality and complexity, and propose to add it to the list of major evolutionary transitions. While transitions to higher‐level units entail the suppression of selection at lower levels, Darwinian immunity re‐opens cell‐level selection within the multicellular organism, under the control of mechanisms that direct, rather than suppress, cell‐level evolution for the benefit of the individual. From a conceptual point of view, the origin of Darwinian immunity can be regarded as the most radical transition in the history of life, in which evolution by natural selection has literally re‐invented itself. Furthermore, the combination of clonal selection and somatic receptor diversity enabled a transition from limited to practically unlimited capacity to store information about the antigenic environment. The origin of Darwinian immunity therefore comprises both a transition in individuality and the emergence of a new information system – the two hallmarks of major evolutionary transitions. Finally, we present an evolutionary scenario for the origin of Darwinian immunity in vertebrates. We propose a revival of the concept of the ‘Big Bang’ of vertebrate immunity, arguing that its origin involved a ‘difficult’ (i.e. low‐probability) evolutionary transition that might have occurred only once, in a common ancestor of all vertebrates. In contrast to the original concept, we argue that the limiting innovation was not the generation of somatic diversity, but the regulatory circuitry needed for the safe operation of amplifiable immune responses with somatically acquired targeting. Regulatory complexity increased abruptly by genomic duplications at the root of the vertebrate lineage, creating a rare opportunity to establish such circuitry. We discuss the selection forces that might have acted at the origin of the transition, and in the subsequent stepwise evolution leading to the modern immune systems of extant vertebrates.     

Evolution and the origin of the visual retinoid cycle in vertebrates

Absorption of a photon by visual pigments induces isomerization of 11-cis-retinaldehyde (RAL) chromophore to all-trans-RAL. Since the opsins lacking 11-cis-RAL lose light sensitivity, sustained vision requires continuous regeneration of 11-cis-RAL via the process called ‘visual cycle’. Protostomes and vertebrates use essentially different machinery of visual pigment regeneration, and the origin and early evolution of the vertebrate visual cycle is an unsolved mystery. Here we compare visual retinoid cycles between different photoreceptors of vertebrates, including rods, cones and non-visual photoreceptors, as well as between vertebrates and invertebrates. The visual cycle systems in ascidians, the closest living relatives of vertebrates, show an intermediate state between vertebrates and non-chordate invertebrates. The ascidian larva may use retinochrome-like opsin as the major isomerase. The entire process of the visual cycle can occur inside the photoreceptor cells with distinct subcellular compartmentalization, although the visual cycle components are also present in surrounding non-photoreceptor cells. The adult ascidian probably uses RPE65 isomerase, and trans-to-cis isomerization may occur in distinct cellular compartments, which is similar to the vertebrate situation. The complete transition to the sophisticated retinoid cycle of vertebrates may have required acquisition of new genes, such as interphotoreceptor retinoid-binding protein, and functional evolution of the visual cycle genes.     

The expression of the dodecameric ferritin in Listeria spp. is induced by iron limitation and stationary growth phase

The new discipline of Evolutionary Developmental Biology (Evo-Devo) is facing the fascinating paradox of explaining morphological evolution using conserved pieces or genes to build divergent animals. The cephalochordate amphioxus is the closest living relative to the vertebrates, with a simple, chordate body plan, and a genome directly descended from the ancestor prior to the genome-wide duplications that occurred close to the origin of vertebrates. Amphioxus morphology may have remained relatively invariant since the divergence from the vertebrate lineage, but the amphioxus genome has not escaped evolution. We report the isolation of a second Emx gene (AmphiEmxB) arising from an independent duplication in the amphioxus genome. We also argue that a tandem duplication probably occurred in the Posterior part of the Hox cluster in amphioxus, giving rise to AmphiHox14, and discuss the structure of the chordate and vertebrate ancestral clusters. Also, a tandem duplication of Evx in the amphioxus lineage produced a prototypical Evx gene (AmphiEvxA) and a divergent gene (AmphiEvxB), no longer involved in typical Evx functions. These examples of specific gene duplications in amphioxus, and other previously reported duplications summarized here, emphasize the fact that amphioxus is not the ancestor of the vertebrates but 'only' the closest living relative to the ancestor, with a mix of prototypical and amphioxus-specific features in its genome.     

Immunocytochemical localization of serotonin in embryos, larvae and adults of the lancelet, Branchiostoma floridae

Serotonin (5-hydroxytryptamine) is a biogenic amine distributed throughout the metazoans and has an old evolutionary history. It is involved as a developmental signal in the early morphogenesis of both invertebrates and vertebrates, whereas in adults it acts mainly as a neurotransmitter and gastrointestinal hormone. In vertebrates, serotonin regulates the morphogenesis of the central nervous system and the specification of serotonergic as well as dopaminergic neurons. The present study uses, as an experimental model, an invertebrate chordate, the lancelet Branchiostoma floridae, characterized by its remarkable homologies with vertebrates that allows the 'bauplan' of the probable ancestor of vertebrates to be outlined. In particular, the involvement of serotonin as a developmental signal in embryos and larvae, as well as a neurotransmitter and gastrointestinal hormone in adult specimens of Branchiostoma floridae, gives further support to a common origin of cephalocordates and vertebrates.     

Vertebrate cranial evolution: Contributions and conflict from the fossil record

In modern vertebrates, the craniofacial skeleton is complex, comprising cartilage and bone of the neurocranium, dermatocranium and splanchnocranium (and their derivatives), housing a range of sensory structures such as eyes, nasal and vestibulo-acoustic capsules, with the splanchnocranium including branchial arches, used in respiration and feeding. It is well understood that the skeleton derives from neural crest and mesoderm, while the sensory elements derive from ectodermal thickenings known as placodes. Recent research demonstrates that neural crest and placodes have an evolutionary history outside of vertebrates, while the vertebrate fossil record allows the sequence of the evolution of these various features to be understood. Stem-group vertebrates such as Metaspriggina walcotti (Burgess Shale, Middle Cambrian) possess eyes, paired nasal capsules and well-developed branchial arches, the latter derived from cranial neural crest in extant vertebrates, indicating that placodes and neural crest evolved over 500 million years ago. Since that time the vertebrate craniofacial skeleton has evolved, including different types of bone, of potential neural crest or mesodermal origin. One problematic part of the craniofacial skeleton concerns the evolution of the nasal organs, with evidence for both paired and unpaired nasal sacs being the primitive state for vertebrates.     

A NEW GENERALIZED PAUCITUBERCULATAN MARSUPIAL FROM THE OLIGOCENE OF BOLIVIA AND THE ORIGIN OF 'SHREW-LIKE' OPOSSUMS

Abstract:  Insights into the origin of 'shrew-like' oposssums of South America are gained thanks to a new fossil from the Oligocene Salla Beds in Bolivia. The specimen described here consists of a partial rostrum, palate and postcanine teeth, and shows several generalized features (cranial and dental) in the context of the Paucituberculata. On this basis we recognize Evolestes hadrommatos gen. et sp. nov. In order to evaluate the affinities of the new taxon, we performed a phylogenetic analysis including representatives of the Caenolestidae, Pichipilus and allies (not regarded here as caenolestids), Palaeothentidae, and Abderitidae, with three outgroups. Evolestes is the basalmost 'caenolestoid', and provides clues to the morphological changes involved in the origin of caenolestids.     

Monophyletic origin of multiple clonal lineages in an asexual fish (Poecilia formosa)

Despite the advantage of avoiding the costs of sexual reproduction, asexual vertebrates are very rare and often considered evolutionarily disadvantaged when compared to sexual species. Asexual species, however, may have advantages when colonizing (new) habitats or competing with sexual counterparts. They are also evolutionary older than expected, leaving the question whether asexual vertebrates are not only rare because of their 'inferior' mode of reproduction but also because of other reasons. A paradigmatic model system is the unisexual Amazon molly, Poecilia formosa, that arose by hybridization of the Atlantic molly, Poecilia mexicana, as the maternal ancestor, and the sailfin molly, Poecilia latipinna, as the paternal ancestor. Our extensive crossing experiments failed to resynthesize asexually reproducing (gynogenetic) hybrids confirming results of previous studies. However, by producing diploid eggs, female F(1) -hybrids showed apparent preadaptation to gynogenesis. In a range-wide analysis of mitochondrial sequences, we examined the origin of P. formosa. Our analyses point to very few or even a single origin(s) of its lineage, which is estimated to be approximately 120,000 years old. A monophyletic origin was supported from nuclear microsatellite data. Furthermore, a considerable degree of genetic variation, apparent by high levels of clonal microsatellite diversity, was found. Our molecular phylogenetic evidence and the failure to resynthesize the gynogenetic P. formosa together with the old age of the species indicate that some unisexual vertebrates might be rare not because they suffer the long-term consequences of clonal reproduction but because they are only very rarely formed as a result of complex genetic preconditions necessary to produce viable and fertile clonal genomes and phenotypes ('rare formation hypothesis').