Top Research of 2012: Developmental Biology

Jump to: Arthropods; Botany; Ecology; Environmental; Evolution; Geology; Historical Geology; Human Evolution; Palaeontology; Zoology.

My subjective picks for the top 10 developmental biology papers of the year, with the caveat that I’m not a developmental biologist by trade, just an avid follower of the field, with my main interest being evo devo and phylogenetic inferences from developmental biology. The master list contains 16 papers. [OA] indicates open access papers.

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10. The making of a fusion branch in the Drosophila trachea.

I summarised the development of the tracheal system in larval Drosophila in this post. This paper fills in the details of the connection between the branches of the tracheal system, at the branching point.

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9. Sequencing and analysis of the gastrula transcriptome of the brittle star Ophiocoma wendtii. [OA]

I gleefully support any research that doesn’t use model organisms. This one fulfils that criterion by using a brittlestar rather than sea urchins. The paper itself is a characterisation of its development and gene expression during gastrulation, and notes the similarities and differences to sea urchins.

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8. Lim homeobox genes in the Ctenophore Mnemiopsis leidyi: the evolution of neural cell type specification. [OA]

This paper studies the expression of Lhx genes in Mnemiopsis leidyi, a ctenophore. Lhx genes are homeobox genes involved in the development of the nervous system – they’re responsible for patterning various types of neurons. There are four of them in this organism, and their expression is diagrammed above. As expected, the expression is concentrated where the most neurons and sensory cells are found. Combined with the phylogenetic analysis in this paper finding that ctenophores and sponges are rather close to each other, this suggests that Lhx first evolved as a way to specify sensory cells: sponges don’t have nerves, but their larvae do have photoreceptive cells that are specified by Lhx. So, in all, this is an important paper for giving us more data to work with when thinking of the original evolution of the nervous system.

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7. Spiral cleavage and early embryology of a loxosomatid entoproct and the usefulness of spiralian apical cross patterns for phylogenetic inferences. [OA]

Entoprocts (also called Kamptozoa) are a phylum of tiny benthic marine invertebrates, suggested by most to be the sister group to the molluscs (the Tetraneuralia hypothesis). This paper studies the development of Loxosomella, a solitary entoproct (species in other families are colonial). It exhibits spiral cleavage along with an apical cross; this confirms that entoprocts belong in the Spiralia. Further analyses in the paper also lend more support for the Tetraneuralia hypothesis.

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6. Segment polarity gene expression in a myriapod reveals conserved and diverged aspects of early head patterning in arthropods.

This paper investigates the expression of several important head patterning genes in the millipede Glomeris marginata. The importance of the paper hinges on the two current leading hypotheses in arthropod phylogeny: the Pancrustacea hypothesis states that insects and crustaceans are sisters, or that insects are crustaceans; and the Atelocerata hypothesis that states that insects and myriapods (millipedes, centiupedes, and their ilk) are sisters. The findings in this paper come out in favour of the Atelocerata – there are several important developmental gene expressions shared between insects and myriapods, but not with crustaceans. Although these could also be explained by convergence.

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5. Unravelling the evolution of neural stem cells in arthropods: Notch signalling in neural stem cell development in the crustacean Daphnia magna.

Notch is one of the most important proteins in animal development. It’s a transmembrane receptor that controls cell-cell communication, and it also coordinates a signalling cascade found in all animals by regulating gene expression – such multitasking by a single protein is very rare. This paper studies Notch signalling in the early nervous system development of a model organism, the water flea Daphnia magna, showing that Notch is key for neuroblast formation (as in vertebrates, which the authors refer to as a case of convergent evolution) and for patterning the ventral neuroectoderm.

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4. Identification of a rudimentary neural crest in a non-vertebrate chordate.

The neural crest has long been considered the key innovation that allowed vertebrates to achieve their evolutionary success. Some authors even go as far as treating it as a fourth germ layer. Basically, the neural crest is a dorsal fold of the neural tube from which a population of migratory multipotent cells is derived. These migrate along specific pathways to form, among other things: the skull and face, teeth, a lot of the heart and circulatory vessels, pigment cells, the spinal column and the peripheral nervous system, and the thyroid and adrenal glands. It’s also long been known that its evolution was not a spontaneous one, but that glimmers of it can be seen in other chordates. This paper is significant in that it identifies more than “glimmers”: it finds that all that’s needed to make a rudimentary neural crest in the tunicate Ciona intestinalis is a misexpression of the a protein called Twist in population of pigment cells in the embryonic head, granting that population migratory abilities identical to those of neural crest cells. This provides a clear scenario for the evolution of the full neural crest of the vertebrates.

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3. What Role Do Annelid Neoblasts Play? A Comparison of the Regeneration Patterns in a Neoblast-Bearing and a Neoblast-Lacking Enchytraeid Oligochaete. [OA]

The neoblasts of annelids should not be confused with neoblasts of planarians: many annelids have no neoblasts and can regenerate just fine, so this paper examines what the true function of annelidan neoblasts is by looking at two closely-related annelids, an asexual one with neoblasts and a sexual one without. It turns out that their role is geared towards making asexual reproduction effective: the sexual species has no neoblasts and has limited regeneration abilities only in the front of the body, whereas the asexual species can regenerate if cut anywhere.

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2. Hox gene expression in the harvestman Phalangium opilio reveals divergent patterning of the chelicerate opisthosoma.

This paper examines the expression of Hox genes in a harvestman, and compares them to the expression in spiders. The biggest differences are found to be in the opisthosome – the back half – of the animals, as seen in B above. It’s those differences that lead to the body plan variability in chelicerates, so this research exposes a new avenue of research for chelicerate evo devo.

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1. Early development of coelomic structures in an echinoderm larva and a similarity with coelomic structures in a chordate embryo.

The drastic form of today’s echinoderms’ body plan (they haven’t always been this screwed up, Recent echinoderms are just a fraction of their past diversity) has always been a stumbling block in the evo devo of deuterostomes. They’re so derived that homologising the structures of echinoderms with chordates is a pretty tentative affair. This paper attempts to do just that by examining the development of the sea urchin Holopneustes purpurescens. It finds that the hydrocoel could be homologous to the notochord, and the coelomic mesoderm homologous to chordate mesoderm, based on the positions of those tissues, as well as gene expression. By extension, this would lead to homologisation of the ambulacra with the chordate body axis. Of course, modern echinoderms have a pentameric body plan; this is explained by duplication. Overall, it’s an interesting and intriguing hypothesis, which is why I place it so high up here (I recommend reading the Discussion section of this paper for the full details). It’s not perfect (I can think of several critiques), but certainly worth considering.

A related paper, not from developmental biology, is Echinoderms Have Bilateral Tendencies: it investigates bilaterian-like behaviour in starfish.

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Jump to: Arthropods; Botany; Ecology; Environmental; Evolution; Geology; Historical Geology; Human Evolution; Palaeontology; Zoology.

Top Research of 2012: Arthropods

Jump to: Botany; Developmental Biology; Ecology; Environmental; Evolution; Geology; Historical Geology; Human Evolution; Palaeontology; Zoology.

Now that we’re done with the top books of the year, let’s look at the top research of the year. I re-examined a total of 412 papers published this year, sorted in the following categories: Arthropods; Botany; Developmental Biology; Ecology; Environmental; Evolution; Geology; Historical Geology; Human Evolution; Palaeontology; and Zoology. As with the books, every day, I will do a top 10 research for each category. The top 10s will be inverted like a proper countdown. As with any top 10 lists, your mileage may vary; these picks and the rankings are all subjective and prone to my own biases.

Let’s start off with the arthropods. The top 10 papers were chosen from a master list of 74 papers. [OA] indicates open access papers. The topic listing, from 10 to 1: spider intelligence; spider silk; fossil insect behaviour; fossil pupation chambers; caste-specific neuroanatomy; early arthropod evolution; evolutionary dynamics; early fossil insect; earliest amber arthropods; treehopper helmet.

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10. The discerning predator: decision rules underlying prey classification by a mosquito-eating jumping spider.

Jumping spiders’ excellent eyesight has led to their also having high intelligence, being able to observe and filter what they see to the point that the African jumping spider Evarcha culicivora can differentiate their prey, female Anopheles mosquitoes, from all other insects flying around just by looking at their antennae. This is what Nelson & Jackson showed with this elegant experiment.

By combining parts from male and female mosquitoes and using the resultant Frankenmosquitoes as lures for the spiders to attack, they identified the two clues that led to the most attacks: a red, blood-engorged abdomen, and slender antennae. Both of these are female mosquito features: male mosquitoes don’t feed on blood (they’re nectar feeders), and males have bushy antennae. As for the specificity for Anopheles mosquitoes, that’s explained by their posture – other mosquitoes rest with their body parallel to the ground, while Anopheles rest with a 45° angle.

For showing that such a tiny spider is capable of such complex prey-distinction and thus giving even more credence to the notion that intelligence is not a function of brain size, as well as for having a great experimental design, Nelson & Jackson get the #10 place.

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9. Post-secretion processing influences spider silk performance.

Spider silk is not a simple strand that’s the same in every species. There’s many different types of silk that come out of different glands, and the silk is also modified after it’s secreted. The study focuses on major ampullate silk, the type of silk that makes up the framework of an orb web and whose stiffness is responsible for the strength of the webs. The researchers examined natural silk, and silk that they supercontracted to remove any post-secretion modifications. What they found was that these supercontracted silks lost the stiff properties of their natural counterparts, meaning that their properties come from whatever modification is made to them, not from the actual structure and composition of the silk. I find this discovery significant because it adds a new dimension to the study of spider silk, a field that has quite a lot of technological and biomimetic research ahead of it.

Other significant spider silk and web-related research this year include:

The role of capture spiral silk properties in the diversification of orb webs: how various silk types affect the web’s properties.

Nonlinear material behaviour of spider silk yields robust webs: This research provides more insight into the factors mentioned above, finding that it isn’t just the type of and modification of silks that affect the web’s properties, but that the geometry of the web is as important in determining its strength and behaviour.

Early Events in the Evolution of Spider Silk Genes [OA]: A phylogeny of genes from the silk-producing glands reveals gene duplications associated with more diverse ecological use of silk and webs.

Functional values of stabilimenta in a wasp spider, Argiope bruennichi: support for the prey-attraction hypothesis: research into the use of stabilimenta, UV-reflective strands of silk that orb-weavers have.

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8. Jurassic mimicry between a hangingfly and a ginkgo from China. [OA]

This is cool more than anything else, and the mimicry is shown in the picture above, from the original paper: A, B, E, and F are gingko leaves; C and H are the described specimen and its wing, D and I are a closely-related species which also exhibits mimesis with gingkos; J and K are gingko leaf closeups. As you can see, the similarities are striking, and the artist’s conception in G shows how well the hangingfly would have blended in. The paper has more details on the coevolution of mimesis between this group of hangingflies and gingkos. In all, a neat piece of work with evolutionary insights as well as cool fossil preservation.

Another paper this year has preserved evidence of insect behaviour: Wing stridulation in a Jurassic katydid (Insecta, Orthoptera) produced low-pitched musical calls to attract females. The mating call of a katydid has been reconstructed based on the preservation of its stridulatory apparatus, a hard file that the wings strike against to make the music. Related, this paper from this year shows how sensitive the hearing of katydids is: Auditory change detection by a single neuron in an insect.

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7. The Earliest Evidence of Holometabolan Insect Pupation in Conifer Wood. [OA]

This paper describes U-shaped burrows in 210 Ma wood from Utah, USA. These were previously assumed to be bee or wasp borings, but the detailed analysis presented in the paper shows that these borings are actually pupation chambers made by a small organism that ate its way into the wood, then emerged from the other side, as presented in the diagram above. From the size of the borings, the authors propose that the organism is a cupedid beetle, showing that these beetles were dominant before the other beetles radiated later.

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6. Division of Labor in the Hyperdiverse Ant Genus Pheidole Is Associated with Distinct Subcaste- and Age-Related Patterns of Worker Brain Organization. [OA]

That different castes will have a different brain organisation is expected and has been shown in many papers (e.g. 1, 2, 3). This paper is significant because it’s so thorough: it examines castes of three species of Pheidole ants and their brain anatomy. The diagram above summarises the pattern observed: the colours are species, the shapes are castes; the axes are two variables that together make up 87% of the brain variation seen. The pattern is clear: neuroanatomy is determined by caste, not by species. This is just underlines the incredible amount of plasticity in ants (and other eusocial insects), where the environment can dictate how an individual will function and develop to allow the colony to adapt to changing needs and conditions.

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5. A Carboniferous Non-Onychophoran Lobopodian Reveals Long-Term Survival of a Cambrian Morphotype.

This paper has equal relevance to palaeontology as it does to arthropods: like several other papers of the past few years (e.g.), it reinforces the idea that the Cambrian freaks didn’t go extinct, but that the nature of the fossil record changes since the Cambrian to make their preservation much rare (the advent of burrowing made it much harder for such soft-bodied forms to be preserved). This one is the most stirking example yet: a long-legged lobopod, 200 million years after the Cambrian (it comes from the famous Mazon Creek locality in Illinois, USA, 296 Ma)! Lobopods are a wastebasket taxon in which soft-bodied arthropods with stubby legs are dumped, including many fossil-only taxa, tardigrades, and onychophorans. There are two groups: short-legged forms (includes the last two) and long-legged ones, up until this paper known only from the Cambrian.

It was a good year for arthropod evolution, with many excellent studies into the biology and diversity of early arthropods:

Exceptionally preserved crustaceans from western Canada reveal a cryptic Cambrian radiation: These Canadian fossils bring the earliest fossil records of branchiopods, copepods, and ostracods back to the mid-Cambrian.

Silurian horseshoe crab illuminates the evolution of arthropod limbs: A horseshoe crab from Herefordshire, showing a very exciting biramous limb, the significance of which would need an entire post to explain.

A Silurian myodocope with preserved soft-parts: cautioning the interpretation of the shell-based ostracod record is another Herefordshire find that finds that ostracod shells, very abundant fossils with significant stratigraphic and other practical use, are not quite as informative taxonomically as previously thought.

Cambrian lobopodians and extant onychophorans provide new insights into early cephalization in Panarthropoda [OA]: A complete redescription of Onychodictyon‘s head, showing that the arthropod mouth may have originated multiple times.

Cambrian bivalved arthropod reveals origin of arthrodization: A new Burgess Shale arthropod suggests that the key feature of arthropods, the exoskeletal segmentation, was a feature that evolved for swimming.

Morphology of Cambrian lobopodian eyes from the Chengjiang Lagerstätte and their evolutionary significance shows that Cambrian lobopods had pretty sophisticated eyesight.

Complex brain and optic lobes in an early Cambrian arthropod: Eyes are nice and all, but how about preserved brains and nervous tissue?

Internal Soft-Tissue Anatomy of Cambrian ‘Orsten’ Arthropods as Revealed by Synchrotron X-Ray Tomographic Microscopy [OA] shows more spectacular internal details of long-extinct arthropods.

Exceptionally Preserved Cambrian Trilobite Digestive System Revealed in 3D by Synchrotron-Radiation X-Ray Tomographic Microscopy [OA]: As above.

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4. Loss of flight promotes beetle diversification. [OA]

In this study, a molecular phylogeny of Japanese carrion beetles was done, and the result found was that flight loss promotes speciation. Flightless populations have more genetic differences between themselves than do flight-enabled populations. This is to be expected: flight enables greater geographic dispersal, allowing distant populations to reproduce and keep gene flow between them; with flight loss, this doesn’t happen, resulting in more isolation and thus more speciation, as shown in the above bar chart. The authors went further and did a short meta-analysis for other beetle groups and found a similar effect. I look forward to deeper studies examining the precise interplay between diversification and flight loss – does flight loss really directly cause speciation, or is it an indirect knock-on effect. Loss of flight must be related to other factors such as habitat requirements, life history, or feeding preferences, as the authors note; maybe it’s those other factors that actually promote the speciation. The authors checked for this in their carrion beetle dataset, but it’s worth looking into with other taxa.

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3. A complete insect from the Late Devonian period.

The fossil doesn’t quite look like an insect until you examine it closely – when I first saw the picture, I thought it was some notostracan. But then it becomes clear that there’s a pair of antennae, then you see the head, then the rest of the body – this is an insect. It’s not the oldest – that honour remains with Rhyniognatha hirsti – but it does come from a time when the fossil record of insects is completely lacking, the Late Devonian, and it’s by far the earliest complete insect – this really is a landmark find.

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2. Arthropods in amber from the Triassic Period.

This is not the oldest amber (that’s from the Carboniferous), but it is the oldest fossiliferous amber. Microorganisms have been reported from it before, but this paper records the oldest arthropod inclusions in amber, beating the previous records from the Middle East by some 100 million years. The arthropods are one fly and two mites (one of which is pictured above), with more still to come in future papers.

Some more cool insect preservation papers published this year include:

The original colours of fossil beetles details how preservation of beetle cuticle allows us to reconstruct the colour of fossil beetles – after all, the metallic sheen that some beetles have isn’t due to pigments, but due to the nanostructure of the cuticle playing tricks with the light. THE CONTROLS ON THE PRESERVATION OF STRUCTURAL COLOR IN FOSSIL INSECTS outlines the details of how cuticle preservation affects recovered colour.

WIDESPREAD PYRITIZATION OF INSECTS IN THE EARLY CRETACEOUS JEHOL BIOTA shows that the insects from Jehol – the famous lacustrine fossil locality that has yielded many feathered dinosaurs – are pyritised with the help of bacterial acitvity.

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1. On Dorsal Prothoracic Appendages in Treehoppers (Hemiptera: Membracidae) and the Nature of Morphological Evidence. [OA]

In 2011, Prud’homme et al. published an intriguing paper with developmental and some morphological evidence that the helmet of treehoppers, pictured above, is actually a cooption of an ancestral wing-like structure. This is obviously a very extraordinary claim, and this paper reviews all the evidence and comes up with alternative scenarios that show flaws in the Prud’homme et al. paper. It gets the top spot not only for the subject matter, but also for being a prime example of the scientific method in action.

A morphology-only critique of the Prud’homme et al. paper was done very early in the year by Yoshizawa [OA].

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Jump to: Botany; Developmental Biology; Ecology; Environmental; Evolution; Geology; Historical Geology; Human Evolution; Palaeontology; Zoology.

“Gradients” and “Fields” in Developmental Biology: A history of the ideas

Anyone who’s taken a course in developmental biology will have heard of “developmental gradients” or “embryonic fields” or “morphogenetic fields”; I learned these in German, so the English names might be different (I’ve seen those three being used). This post is about the history of these ideas of fields and gradients in developmental biology.

The Rise of Animals

This talk will take us through the origin and initial diversifications of animal life.

It will be chronological, from the latest Neoproterozoic to the end of the Palaeozoic. Wikipedia has a timeline for you to orient yourself.

One theme that will be very prominent throughout is that of Konservat Lagerstätten, or sites of exceptional fossil preservation. Whereas 99% of the fossil record consists of bones, shells, teeth and other hard parts, these localities preserve soft parts, such as muscle and tissue. We will see just how important this is in general for palaeontology, but also in the study of this particular topic of the origin of animals.

Generation of Mammalian Coat Patterns

There are several theories, all supported by some pretty sophisticated mathematics, that can explain the generation of coat patterns. As far as I know, the one that is generally the most accepted is the one developed by Murray (1989), which is based on the principle of Turing bifurcation and the positional informational theory by developmental biologist Lewis Wolpert (Wolpert, 1981).

Annelida: A Note on Spiralian Development

For a nicely-formatted and better referenced PDF of the entire series, click here!

An important feature that has played a large role in the quest to place annelids within the system of the Metazoa is their development. They undergo spiral cleavage, a presumed highly-conserved form of development that is also found in molluscs, sipunculids, echiurans, nemerteans, myzostomids, ectoprocts, some flatworms and maybe gnathostomulids, and some have used spiral cleavage as an autapomorphy to unite these taxa under a single monophyletic Spiralia taxon (first proposed by Schleip in his 1929 book “Die Determination der Primitiventwicklung”). We will look at this in more detail in the next post.

Vertebrate Heads: Development

Neural Crest Formation. Sauka-Sprenger & Bronner-Fraser (2008).

Let’s start from the very beginning, as this can be simply retold step by step as a story. It’s useful to keep the picture above open in a tab. The very first step is the induction of the neural plate, which is simply a sheet of neuron progenitor cells derived from the ectoderm – those ectodermal cells that don’t go into the neural plate will later become the epidermis. The specification of the neural plate cells happens pretty early during gastrulation, under the action of several signalling molecules (they’re different in every vertebrate lineage).

Deep Homology

Darwin referred to the products of evolution as ‘endless forms most beautiful’. Disparity (the word meaning “diversity of morphology”) can be classified: “All mammals have titties” is a valid biological statement. But within all this disparity lie unifying characters: all mammals have boobs, but they also have a backbone; frogs have a backbone too, so that’s a common trait. But a tadpole (baby frog) does not look like a frog at all; developmental biology and ontogeny also greatly increase disparity.

Developmental Plasticity

Before starting, a small note: I currently have 4 time-consuming projects running in parallel, so updates will be sporadic. Sorry.

In this post, we’ll look at how the environment can influence development, including phenotypic plasticity (what is an ecomorph?) and epigenetics. Also, for the first time ever, I will put in a reference and further reading list at the end.