Inversion (evolutionary biology)
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evolutionary developmental biology Evolutionary developmental biology (informally, evo-devo) is a field of biological research that compares the developmental processes of different organisms to infer how developmental processes evolved. The field grew from 19th-century beginni ...
, inversion refers to the hypothesis that during the course of animal evolution, the structures along the
dorsoventral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek roots, describe something in its standard anatomical position. This position prov ...
(DV) axis have taken on an orientation opposite that of the ancestral form. Inversion was first noted in 1822 by the French zoologist
Étienne Geoffroy Saint-Hilaire Étienne Geoffroy Saint-Hilaire (15 April 177219 June 1844) was a French naturalist who established the principle of "unity of composition". He was a colleague of Jean-Baptiste Lamarck and expanded and defended Lamarck's evolutionary theories. ...
, when he dissected a
crayfish Crayfish are freshwater crustaceans belonging to the clade Astacidea, which also contains lobsters. In some locations, they are also known as crawfish, craydids, crawdaddies, crawdads, freshwater lobsters, mountain lobsters, rock lobsters, mu ...
(an
arthropod Arthropods (, (gen. ποδός)) are invertebrate animals with an exoskeleton, a Segmentation (biology), segmented body, and paired jointed appendages. Arthropods form the phylum Arthropoda. They are distinguished by their jointed limbs and Arth ...
) and compared it with the
vertebrate Vertebrates () comprise all animal taxa within the subphylum Vertebrata () ( chordates with backbones), including all mammals, birds, reptiles, amphibians, and fish. Vertebrates represent the overwhelming majority of the phylum Chordata, ...
body plan A body plan, ( ), or ground plan is a set of morphological features common to many members of a phylum of animals. The vertebrates share one body plan, while invertebrates have many. This term, usually applied to animals, envisages a "blueprin ...
. The idea was heavily criticised, but periodically resurfaced, and is now supported by some molecular embryologists.


History

As early as 1822, the French zoologist
Étienne Geoffroy Saint-Hilaire Étienne Geoffroy Saint-Hilaire (15 April 177219 June 1844) was a French naturalist who established the principle of "unity of composition". He was a colleague of Jean-Baptiste Lamarck and expanded and defended Lamarck's evolutionary theories. ...
noted that the organization of
dorsal Dorsal (from Latin ''dorsum'' ‘back’) may refer to: * Dorsal (anatomy), an anatomical term of location referring to the back or upper side of an organism or parts of an organism * Dorsal, positioned on top of an aircraft's fuselage * Dorsal c ...
and
ventral Standard anatomical terms of location are used to unambiguously describe the anatomy of animals, including humans. The terms, typically derived from Latin or Greek language, Greek roots, describe something in its standard anatomical position. Th ...
structures in
arthropod Arthropods (, (gen. ποδός)) are invertebrate animals with an exoskeleton, a Segmentation (biology), segmented body, and paired jointed appendages. Arthropods form the phylum Arthropoda. They are distinguished by their jointed limbs and Arth ...
s is opposite that of
mammal Mammals () are a group of vertebrate animals constituting the class Mammalia (), characterized by the presence of mammary glands which in females produce milk for feeding (nursing) their young, a neocortex (a region of the brain), fur or ...
s. Five decades later, in light of Darwin's theory of "descent with modification", German zoologist
Anton Dohrn Felix Anton Dohrn FRS FRSE (29 December 1840 – 26 September 1909) was a prominent German Darwinist and the founder and first director of the first zoological research station in the world, the Stazione Zoologica in Naples, Italy. He worked ...
proposed that these groups arose from a
common ancestor Common descent is a concept in evolutionary biology applicable when one species is the ancestor of two or more species later in time. All living beings are in fact descendants of a unique ancestor commonly referred to as the last universal comm ...
which possessed a body plan similar to that of modern
annelid The annelids (Annelida , from Latin ', "little ring"), also known as the segmented worms, are a large phylum, with over 22,000 extant species including ragworms, earthworms, and leeches. The species exist in and have adapted to various ecol ...
s with a
ventral nerve cord The ventral nerve cord is a major structure of the invertebrate central nervous system. It is the functional equivalent of the vertebrate spinal cord. The ventral nerve cord coordinates neural signaling from the brain to the body and vice versa, in ...
and dorsal heart. Whereas this arrangement is retained in
arthropod Arthropods (, (gen. ποδός)) are invertebrate animals with an exoskeleton, a Segmentation (biology), segmented body, and paired jointed appendages. Arthropods form the phylum Arthropoda. They are distinguished by their jointed limbs and Arth ...
s and other
protostome Protostomia () is the clade of animals once thought to be characterized by the formation of the organism's mouth before its anus during embryonic development. This nature has since been discovered to be extremely variable among Protostomia's memb ...
s, in
chordate A chordate () is an animal of the phylum Chordata (). All chordates possess, at some point during their larval or adult stages, five synapomorphies, or primary physical characteristics, that distinguish them from all the other taxa. These fiv ...
deuterostome Deuterostomia (; in Greek) are animals typically characterized by their anus forming before their mouth during embryonic development. The group's sister clade is Protostomia, animals whose digestive tract development is more varied. Some exampl ...
s, the nerve cord is located dorsally and the heart ventrally. The inversion hypothesis was met with scornful criticism each time it was proposed, and has periodically resurfaced and been rejected. However, some modern molecular embryologists suggest that recent findings support the idea of inversion.


Evidence for inversion

In addition to the simple observation that the dorsoventral axes of protostomes and chordates appear to be inverted with respect to each other,
molecular biology Molecular biology is the branch of biology that seeks to understand the molecular basis of biological activity in and between cells, including biomolecular synthesis, modification, mechanisms, and interactions. The study of chemical and physi ...
provides some support for the inversion hypothesis. The most notable piece of evidence comes from analysis of the
gene In biology, the word gene (from , ; "...Wilhelm Johannsen coined the word gene to describe the Mendelian units of heredity..." meaning ''generation'' or ''birth'' or ''gender'') can have several different meanings. The Mendelian gene is a ba ...
s involved in establishing the DV axis in these two groups. In the fruit fly ''
Drosophila melanogaster ''Drosophila melanogaster'' is a species of fly (the taxonomic order Diptera) in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly" or "pomace fly". Starting with Ch ...
'', as well as in other protostomes, the β-type transforming growth factor (
TGF-β Transforming growth factor beta (TGF-β) is a multifunctional cytokine belonging to the transforming growth factor superfamily that includes three different mammalian isoforms (TGF-β 1 to 3, HGNC symbols TGFB1, TGFB2, TGFB3) and many other sign ...
) family member ''
decapentaplegic Decapentaplegic (Dpp) is a key morphogen involved in the development of the fruit fly ''Drosophila melanogaster'' and is the first validated secreted morphogen. It is known to be necessary for the correct patterning and development of the early ' ...
'' (''dpp'') is expressed dorsally and is thought to suppress neural fate. On the ventral side of the embryo, a ''dpp'' inhibitor, ''short gastrulation'' (''sog''), is expressed, thus allowing nervous tissue to form ventrally. In chordates, the ''dpp''
homolog In biology, homology is similarity due to shared ancestry between a pair of structures or genes in different taxa. A common example of homologous structures is the forelimbs of vertebrates, where the wings of bats and birds, the arms of prima ...
BMP-4 Bone morphogenetic protein 4 is a protein that in humans is encoded by ''BMP4'' gene. BMP4 is found on chromosome 14q22-q23. BMP4 is a member of the bone morphogenetic protein family which is part of the transforming growth factor-beta superfam ...
is expressed in the prospective ventral (non-neural) part of the embryo while several ''sog''-like BMP inhibitors ( Chordin,
Noggin Noggin may refer to: General * Noggin or gill (volume), a unit of volume * Noggin (cup), a small cup * Noggin, slang for head A head is the part of an organism which usually includes the ears, brain, forehead, cheeks, chin, eyes, nose, an ...
,
Follistatin Follistatin also known as activin-binding protein is a protein that in humans is encoded by the ''FST'' gene. Follistatin is an autocrine glycoprotein that is expressed in nearly all tissues of higher animals. Its primary function is the binding ...
) are expressed dorsally. Other patterning genes also show conserved domains of expression. The neural patterning genes ''vnd'', ''ind'', ''msh'', and ''
netrin Netrins are a class of proteins involved in axon guidance. They are named after the Sanskrit word "netr", which means "one who guides". Netrins are genetically conserved across nematode worms, fruit flies, frogs, mice, and humans. Structurally, ...
'' are expressed in the ''Drosophila'' ventral nerve cells and midline mesectoderm. The chordate
homologs A couple of homologous chromosomes, or homologs, are a set of one maternal and one paternal chromosome that pair up with each other inside a cell during fertilization. Homologs have the same genes in the same loci where they provide points alon ...
of these genes, NK2, Gsh1/2, Msx1/3, and
Netrin Netrins are a class of proteins involved in axon guidance. They are named after the Sanskrit word "netr", which means "one who guides". Netrins are genetically conserved across nematode worms, fruit flies, frogs, mice, and humans. Structurally, ...
, are expressed in the dorsal
neural tube In the developing chordate (including vertebrates), the neural tube is the embryonic precursor to the central nervous system, which is made up of the brain and spinal cord. The neural groove gradually deepens as the neural fold become elevated, a ...
. Furthermore, the tinman/Nkx2-5 gene is expressed very early in cells that will become the
heart The heart is a muscular organ in most animals. This organ pumps blood through the blood vessels of the circulatory system. The pumped blood carries oxygen and nutrients to the body, while carrying metabolic waste such as carbon dioxide t ...
in both ''Drosophila'' (dorsally) and chordates (ventrally). Additional support comes from work on the development of the
polychaete Polychaeta () is a paraphyletic class (biology), class of generally marine invertebrate, marine annelid worms, common name, commonly called bristle worms or polychaetes (). Each body segment has a pair of fleshy protrusions called parapodia that ...
annelid The annelids (Annelida , from Latin ', "little ring"), also known as the segmented worms, are a large phylum, with over 22,000 extant species including ragworms, earthworms, and leeches. The species exist in and have adapted to various ecol ...
''
Platynereis dumerilii ''Platynereis dumerilii'' is a species of annelid polychaete worm. It was originally placed into the genus ''Nereis'' and later reassigned to the genus '' Platynereis''. ''Platynereis dumerilii'' lives in coastal marine waters from temperate t ...
'', another protostome. Even more so than ''Drosophila'', its pattern of central-nervous-system development is strikingly similar to that of vertebrates, but inverted. There is also evidence from left-right asymmetry. Vertebrates have a highly conserved Nodal signaling pathway that acts on the left side of the body, determining left-right asymmetries of internal organs.
Sea urchin Sea urchins () are spiny, globular echinoderms in the class Echinoidea. About 950 species of sea urchin live on the seabed of every ocean and inhabit every depth zone from the intertidal seashore down to . The spherical, hard shells (tests) of ...
s have the same signaling pathway, but it acts on the right side of the body. It was even shown that an opposing right-sided signal for regulating left-right asymmetry in vertebrates, i.e. BMP signaling pathway, is activated on the left side of the sea urchin larva, suggesting an axial inversion during evolution from basal deuterostome to chordate such like amphioxus. Because in amphioxus, Nodal signaling pathway is on the left side of the embryo, which is the same situation as vertebrates. Sea urchins, like other echinoderms, have radially-symmetric adults, but bilaterally-symmetric larvae. Since sea urchins are deuterostomes, this suggests that the ancestral deuterostome shared its orientation with protostomes, and that dorsoventral inversion originated in some ancestral chordate. There is evidence that invertebrate chordates are also inverted.
Ascidian Ascidiacea, commonly known as the ascidians, tunicates (in part), and sea squirts (in part), is a polyphyletic class in the subphylum Tunicata of sac-like marine invertebrate filter feeders. Ascidians are characterized by a tough outer "tunic" m ...
larvae have a dorsal mouth, as one would expect from inversion. The
amphioxus The lancelets ( or ), also known as amphioxi (singular: amphioxus ), consist of some 30 to 35 species of "fish-like" benthic filter feeding chordates in the order Amphioxiformes. They are the modern representatives of the subphylum Cephalochorda ...
has an odd feature: its mouth appears on the left side and migrates to the ventral side. Biologist Thurston Lacalli speculates that this may be a recapitulation of the migration of the mouth from the dorsal to the ventral side in a protochordate.


Hemichordates: an intermediate body plan?

Some biologists have proposed that the
Hemichordates Hemichordata is a phylum which consists of triploblastic, enterocoelomate, and bilaterally symmetrical marine deuterostome animals, generally considered the sister group of the echinoderms. They appear in the Lower or Middle Cambrian and includ ...
(specifically the
Enteropneusta The acorn worms or Enteropneusta are a hemichordate class of invertebrates consisting of one order of the same name. The closest non-hemichordate relatives of the Enteropneusta are the echinoderms. There are 111 known species of acorn worm in the ...
) may represent an intermediate body plan in the evolution of the "inverted" state of the chordates. Though they are considered deuterostomes, the dorsoventral axis of hemichordates retains features of both protostomes and chordates. For example, enteropneusts have an
ectoderm The ectoderm is one of the three primary germ layers formed in early embryonic development. It is the outermost layer, and is superficial to the mesoderm (the middle layer) and endoderm (the innermost layer). It emerges and originates from t ...
ally-derived dorsal nerve cord in the collar region which has been proposed to be homologous to the chordate neural tube. However, they also have a ventral nerve cord and a dorsal contractile vessel similar to protostomes. Furthermore, the relative positions other "intermediate" structures in hemichordates, such as the hepatic organs and ventral pygochord, which has been proposed to be homologous to the chordate-defining
notochord In anatomy, the notochord is a flexible rod which is similar in structure to the stiffer cartilage. If a species has a notochord at any stage of its life cycle (along with 4 other features), it is, by definition, a chordate. The notochord consis ...
, are retained but inverted. Nübler-Jung and Arendt argue that the principal innovation in the chordate lineage was the obliteration of the mouth on the neural side (as in hemichordates, arthropods, and annelids) and the development of a new mouth on the non-neural ventral side.


Alternative hypotheses

While the idea of dorsoventral axis inversion appears to be supported by morphological and molecular data, others have proposed alternative plausible hypotheses (reviewed in Gerhart 2000). One assumption of the inversion hypothesis is that the common ancestor of protostomes and chordates already possessed an organized central nervous system located at one pole of the dorsoventral axis. Alternatively, this ancestor may have possessed only a diffuse nerve net or several bundles of nervous tissue with no distinct dorsoventral localization. This would mean that the apparent inversion was simply a result of concentration of the central nervous system at opposite poles independently in the lineages leading to protostomes and chordates. Lacalli (1996) suggested a scenario in which the ancestor had a single opening to the digestive system, and that the neural and non-neural mouths arose independently in protostomes and chordates, respectively. By this hypothesis, there is no need for inversion. Martindale and Henry propose a ctenophore-like ancestor (biradial rather than bilateral) with a concentrated nerve cord and two anal pores on opposite sides of the animal in addition to a terminal gut opening. If one of these pores became the mouth in protostomes and the other became the mouth in deuterostomes, this would also preclude inversion. Another alternative, proposed by von Salvini-Plawen, states that the ancestor had a two-part nervous system - one part concentrated, the other diffuse. The nervous systems of protostome and deuterostome descendants of this ancestor may have arisen independently from these two distinct parts. Axial twist theories propose that not the whole body, but only the anterior region of the head is inverted. These theories by Kinsbourne and de Lussanet & Osse also explain the presence of an optic chiasm in vertebrates and the contralateral organization of the
forebrain In the anatomy of the brain of vertebrates, the forebrain or prosencephalon is the Anatomical terms of location#Directional terms, rostral (forward-most) portion of the brain. The forebrain (prosencephalon), the midbrain (mesencephalon), and hin ...
. One of these theories is supported by
developmental Development of the human body is the process of growth to maturity. The process begins with fertilization, where an egg released from the ovary of a female is penetrated by a sperm cell from a male. The resulting zygote develops through mitosi ...
evidence and even explains the asymmetric organization of the
heart The heart is a muscular organ in most animals. This organ pumps blood through the blood vessels of the circulatory system. The pumped blood carries oxygen and nutrients to the body, while carrying metabolic waste such as carbon dioxide t ...
and
bowels The gastrointestinal tract (GI tract, digestive tract, alimentary canal) is the tract or passageway of the digestive system that leads from the mouth to the anus. The GI tract contains all the major organs of the digestive system, in humans ...
.


References


External links


An explanation of DV patterning in ''Drosophila''

P.Z. Myers on axis inversion and hemichordates

P.Z. Myers on axis inversion and annelids: "We have the brains of worms"
{{DEFAULTSORT:Inversion (Evolutionary Biology) Developmental biology Evolutionary biology Evolutionary developmental biology