The Gender of a Table

During the nomenclature section of last week's Systematics Workshop, there seemed to be one detail that, going by people's questions afterwards, seemed to cause the most confusion. This was the question of species name formation and gender agreement. I thought it would be helpful to give a (relatively) brief explanation of how this works.

The current system of species nomenclature is the binomial system, where every species is referred to by a genus and species name. Traditionally, these names have been derived from Latin or Greek, and even if not directly derived from Latin they are treated as if they were. Effectively, the binomen is a brief Latin phrase referring to a given species. Thus, Canis is a "dog", Canis familiaris (the domestic dog) is the "familiar dog". Lumbricus is an "earthworm", Lumbricus terrestris is the "terrestrial earthworm". Where this gets a little complicated for English speakers is that, unlike English, Latin (as well as Greek) is an inflecting language, where the form of words (usually the ending) changes to indicate their position and role in a sentence. The other major difference between Latin and English is that nouns in Latin (and Greek) have a fixed gender (masculine, feminine or neuter) that can affect their formation and sometimes the formation of words around them. It is important to realise that nouns may have a grammatical gender even if the object the word refers to does not have an actual gender. For instance "tabula" (table) is grammatically feminine, even though a table is obviously not actually female.

The name of a genus is always treated as a singular noun in the nominative case (that is, the case that would be used for the subject of a sentence)*. The species name can be an adjective or a noun in apposition** (in Latin, an adjective comes after the noun it refers to, which is why the species name follows the genus name). A "noun in apposition" is a noun that is being used as an adjective. For instance, in the phrase "small foot", the word "foot" is a noun and has the same grammatical role as a genus name in a binomen, while the word "small" is an adjective. However, in the phrase "elephant foot", the word "elephant" is a noun in apposition - it is a noun in its own right that is here playing the role of an adjective. In English, the distinction is generally not too significant (except, of course, we can change word order to say "the foot is small" but not "the foot is elephant"), but in Latin it makes more difference. Adjectives in Latin do not have fixed genders of their own - instead, an adjective will generally vary in form according to gender, and the gender and case of the adjective must agree with that of the noun it refers to. For instance, "tardus" is the masculine form of the Latin word for "slow". Were we to refer to a "slow man" (the Latin word for "man", funnily enough, being masculine), we would refer to a "vir tardus". However, if we were referring to a "slow woman", then the phrase concerned would be a "femina tarda" - note the change in the form of the adjective. Nouns in apposition, in contrast, do have their own fixed gender and hence do not chance to match the gender of the noun they refer to. Dusty Springfield may have been impressed by the son of a vir evangelizator, but she could have also considered the son of a femina evangelizator***. Whether a species name is an adjective or a noun in apposition is also important if the species is transferred to a new genus whose name differs in gender from that of the original genus. If the species name is an adjective, it has to change to match the gender of the new genus. If it is a noun in apposition, it does not change.

*In proper Latin, the form of a word would change depending on whether it was subject, object or some other factor in a sentence. For biological names, the role of inflection has been limited to the name itself, and you needn't concern yourself with its role in the larger sentence. For instance, it is correct to say "I saw a Tyrannosaurus rex", not "I saw a Tyrannosaurum regem".

**It may also be a verb participle - that is, the form of a verb that functions as an adjective (for instance, the "sleeping" in the phrase "sleeping dog"). The rules for verb participles are effectively the same as those for adjectives.

***Though it has to be admitted that the clash of genders give the latter phrase an inherent awkwardness in Latin that wouldn't exist in its English equivalent. It is linguistic differences like this that often make verbal humour so bloody difficult to translate from one language to another, while a custard pie is universal.



If the species name is an adjective, it is always in the nominative case to match the genus name. However, if the species name is a noun in apposition, it may be in either the nominative or the genitive (the possessive) case. The most common use of the genitive is if the species is named after someone - for instance, Gorilla graueri (the eastern lowland gorilla) is "Grauer's gorilla". Other uses of the genitive include cases where a parasite may be named after the host it was found on - for instance, the fish parasite Myxobolus cyprini would have been found on a carp (Cyprinus). The form of the genitive, of course, is determined by the rules of Latin grammar (note that singular and plural genitive forms differ from each other - from hereon in, references to the genitive form only refer to the singular, but authors do sometimes have cause to use the plural), and derives solely from the source of the species name - it is not affected by the genus name. It has become common practice to give the name of a species named after a person a masculine or feminine ending depending on whether the person being honoured is male or female*. There is no conflict whatsoever in placing a feminine possessive species name in a masculine genus - no more so than a gender conflict would exist in the English phrase "Julia's husband".

*This was not always necessarily the case - surnames used to be treated as masculine regardless of whether the person whose surname it was was a man or a woman. Conflicts have arisen from the change in practice when some authors have "corrected" older names honouring women but given masculine forms. Needless to say, the question of whether 'tis better to correct the effects of perceived past gender discrimination or to maintain established usage and spelling is a touchy subject that I'm leaving well alone for now.

When you look up a noun in a Latin dictionary, such as "woman", you'll see something like "femina, -ae. f." This indicates that the word for woman has the nominative form "femina" and its possessive form is "feminae", while the "f." indicates that the word is feminine. Latin nouns are divided into five "declensions", with each declension having its own set of case endings. The genitive (possessive) ending is given in the dictionary to indicate which declension the word belongs to, because the nominative ending varies more between words in a declension than genitive does. The genitive form also indicates the stem of the word to which the case endings are appended or which is used to form compound words if the stem is not clear from the nominative (for instance, "king" would be listed as "rex, regis" - the stem of rex is reg-, which is why we have "regicide" rather than "rexicide"). First declension words usually end in "-a", are usually feminine, and have the genitive ending "-ae". Second declension words end in "-us" (generally masculine) or "-um" (neuter) and have the genitive ending "-i". Third declension has no standard nominative ending, but genitive forms end in "-is" (apart from a few words derived from Greek with genitives that end in "-os"). Fourth declension nouns may be any gender, with masculine and feminine words ending in "-us" and neuter words in "-u", while genitive ends in "-us". Fifth declension names are usually feminine and end in "-es" with genitive ending in "-ei". In the majority of cases, though, a name ending in "-us" will be masculine, one ending in "-a" will be feminine, and one ending in "-um" will be neuter. If the genus name comes from any language other than Latin or Greek, then similar guidelines are recommended - names ending in "-us" should be treated as masculine, those ending in "-a" should be made into feminine genera, while most other endings should be treated as neuter. There are some exceptions to the above - for instance, "agricola, -ae" (farmer) is a first declension word ending in "-a", but is actually masculine, while "crus" (lower leg) might look at first glance like a masculine second declension word, but is actually a neuter third declension word with genitive "cruris"*. (And while I'm discussing dictionaries, I'd like to send an enormous "thank you" to the compilers of Perseus Tools. This is an absolutely fantastic resource with online searchable Latin and Greek dictionaries and grammars. It sometimes runs at the speed of continental drift, and can be a little temperamental, but there have been a number of times lately that I couldn't have done without it.)

*This last example has actually been my personal bane - one of the genera I work on is called Spinicrus and I have to continually remind myself that it's a neuter name, not a masculine one. When I published a checklist of described species of Megalopsalidinae (Opiliones) a few years ago, I corrected two species names that had been originally published in the masculine form to their appropriate neuter forms - then inadvertently wrote down two other names that had so far been correctly spelt as neuters in inaccurate masculine forms. Needless to say, I didn't notice my mistake until the published journal arrived in my mailbox.

Latin adjectives fall into two classes, one of which follows third declension while the other follows first and second declensions. First/second declension adjectives end in "-us", "-a" or "-um" for masculine, feminine or neuter forms respectively. Third declension adjectives do not differ between masculine and feminine, but do have different neuter forms - for instance, the word for slender is "gracilis" if masculine or feminine, but "gracile" if neuter. Dictionary entries for adjectives will give the masculine form followed by the feminine (if different) then neuter endings, e.g. "magnus, -a, -um" ("large") or "gracilis, -e".



Needless to say, there are cases where it may be difficult to discern how to treat a given case. It may be difficult to distinguish whether a species name is meant to be an adjective or a noun in apposition - "small foot" and "elephant foot" may be fairly clear, but what should we make of "human foot"? Most modern species descriptions will explain the derivation of a new species name, but this has not always been the case in the past. I'm not sure how the botanical and bacterial codes handle such cases, but the zoological code requires that in such cases the species name be assumed to be a noun in apposition and not subject to gender change if the genus changes. Similarly, if it is not clear whether a genus name is supposed to be masculine, feminine or neuter, the gender should be assumed according to the guidelines for non-Latin names explained above. In some cases that have been persistently confusing in the past, the zoological code mandates blanket solutions - names ending in "-cola" are masculine regardless of derivation, while names ending in "-ops" are masculine even if they were originally treated as feminine.

The suggestion has been made in the past that in light of the growing distance between biological names and their supposed Latin origins, as well as the general abandonment of Latin learning and usage, grammatical gender issues should be dropped for biological nomenclature. A species name, it is argued, should not have to change simply because the genus name does. This is a complicated issue, but I would like to point out that (A) it is only to speakers of non-gendered languages such as English that the process seems complicated. Conversely, to native speakers of gendered languages such as French, the idea of simply ignoring proper word formation borders on the obscene, not to mention the cacophonous; (B) not requiring genus and species names to agree in gender could potentially be even more confusing than the current situation, as instead of having general guidelines authors would have to remember the correct formation for every single name; and (C) many hundreds of species names have changed in the past as they were transferred between genera - what are to become of them (especially if they haven't held their original gender since some time in the 1700s)?

Picture Credits: Tweedledum and Tweedledee from Through the Looking Glass, and what Alice found there by Lewis Carroll (1871).

Spread from a mid-14th century edition of De Materia Medica by Dioscorides, originally written in the first century AD.

"The Pilgrim" from The Innocents Abroad by Mark Twain (1869).

Clocking Up Carnivalia

Two recent carnivals of note, both of them at A Blog Around the Clock:

Berry Go Round brings you the latest news from the world of sessile photosynthetic eukaryotes (aka plants).

The Giant's Shoulders is a new carnival collecting reviews and commentaries on "classic" science publications. This is a fantastic idea - scientific progress does not occur in a cultural vacuum, and it is important to appreciate the history of scientific progress (or, in a few cases, regress). As a palaeontologist might potentially put it, "Those who do not know George Gaylord Simpson are doomed to make a twat of themselves by bringing up 'new' questions that were being argued about fifty years ago".

I's Been Ejucated, now I Can Haz Snails Pleez? Kthnx

The National Postgraduate Taxonomy Workshop has been and gone, and I arrived back late on Friday evening from a fun and very full week that definitely constituted time well spent. A full range of students was represented, working on taxa from algae to arthropods, myxosporeans to mosses, podocarps to Platypterygius, frogs to fungi. The presentations were exceedingly helpful, though by about midway through the week my head was feeling so crammed full of information that I feared that moving my head to quickly would cause my brain to slosh out from my ears. Highlights for me included getting a better understanding of what a Bayesian analysis actually does (something that, to be quite honest, I'd heretofore been a little fuzzy about), a very helpful presentation from the editor of one of the high-level Australian systematics journals on effective methods for presenting and processing article manuscripts and revisions, and discussion on the future of taxonomic research and how best to secure that future. As expected, the workshop was a fantastic resource in a time when formal taxonomic training has become something of a rarity, and I believe all the students involved were unanimous in urging that such workshops become a regular occurrence.


Cepaea nemoralis, a highly variable terrestrial snail that has long been a model organism in heredity studies. Image via Palaeos.

But now things must return to normality, and it being Monday it's time for a Taxon of the Week post. The last such post two weeks ago was on the fossil gastropod family Scoliostomatidae, and this week's highlight post continues with that gooey molluscan goodness with another group of gastropods, the Stylommatophora. While you may not be familiar with the name, Stylommatophora are actually the most instantly recognisable of all gastropod groups, for this is the group that includes the significant majority of land snails. Aydin Örstan has recently presented a series of posts discussing the difficulties of classing many gastropods (or other moisture-associated organisms for that matter) as "terrestrial" or "aquatic", so I should probably qualify that last statement by stressing that "land snails" here refers to fully terrestrialised taxa that do not have an aquatic component to their life cycle. The name "Stylommatophora" refers to what must be the second thing that any child learns about snails (after learning that they carry their house on their back), that their eyes are on the end of stalks. More than one group of stylommatophorans has reduced or lost the shell - these, of course, are the slugs and semi-slugs (yes, "semi-slug" is a valid term, though unfortunately, to the best of my knowledge "slugi" is not). Such shell loss has occured multiple times. The most influential classification of stylommatophorans was the 1900 classification by Pilsbry that divided them into three groups based on the anatomy of the excretory system, the Orthurethra, Sigmurethra and Heterurethra. Pilsbry regarded the orthurethran straight ureter as ancestral to the sigmurethran sigmoid ureter, but more recent molecular phylogenies have supported the reverse - orthurethrans are a monophyletic group within the paraphyletic "sigmurethrans", with the earliest division within the stylommatophorans being between the "achatinoid" and "non-achatinoid" clades (Wade et al., 2001, 2006). The Elasmognatha (≈Heterurethra) are a small group of two families, the shelled Succineidae and shell-less Athoracophoridae, whose status as a monophyletic group is well-supported but whose position relative to other stylommatophorans is not.


The giant African snail Achatina fulica, one of the largest terrestrial gastropods. Photo by Roberta Zimmerman. Introduced populations of Achatina snails (often imported for food) have become a serious problem in some parts of the world. Interestingly, snails are generally attracted to calcium, and chalk-based baits have often been used in their control. I once lived in a rather damp and disgusting house that had a problem with slugs crawling into the pantry through openings in the base. Once there they would invariably make a beeline direct for the flour. I still don't really know why.

This newer division into achatinoids and non-achatinoids does not appear to be well-supported morphologically, though non-achatinoids tend to have better developed copulatory organs than achatinoids. For instance, those families with members that inject each other with calcareous "love darts" are all non-achatinoids. However, it is debatable whether and to what to degree this represents phylogenetic versus functional considerations. All stylommatophorans are functional hermaphrodites, but mating behaviour differs between taxa that mate face-to-face and inseminate each other simultaneously or those in which one individual mounts the other and insemination may be simultaneous, sequential or unilateral. As well as only occurring in achatinoids, love-darting only occurs in face-to-face copulators - and all face-to-face copulators are non-achatinoids. The function of the love darts is poorly known, but studies in Helix aspersa have shown that they induce faster uptake of received sperm by the darted individual, and one of the leading suggestions is that they discourage reproductive "cheats" that attempt to donate sperm while not taking up their partner's. Such behaviour is really only a consideration in species that inseminate simultaneously, and while many achatinoids do have simultaneous insemination their shell-mounting behaviour may be less conducive to forcing reciprocity in sperm uptake (Davison et al., 2005).


Triboniophora graeffei, an athoracophorid slug. The large hole visible behind the head is the opening to the lung. Photo by Bill Rudman.

Their fully terrestrial habits (not to mention the absence of a shell in many species) mean that stylommatophorans have a much poorer fossil record than other gastropods, and their time of origin is a little doubtful. While Solem & Yochelson assigned some Carboniferous and Permian fossil snails to extant stylommatophoran families, this assignation is not well-supported and the next record of land snails is not until over 100 million years later in the Cretaceous (Wade et al., 2006). As discussed in the scoliostomatid post, the elucidation of relationships between Palaeozoic and later gastropods and distinguishing true relationships from convergences is generally a process fraught with difficulty.

REFERENCES

Davison, A., C. M. Wade, P. B. Mordan & S. Chiba. 2005. Sex and darts in slugs and snails (Mollusca: Gastropoda: Stylommatophora). Journal of Zoology 267 (4): 329-338.

Wade, C. M., P. B. Mordan & B. Clarke. 2001. A phylogeny of the land snails (Gastropoda: Pulmonata). Proceedings of the Royal Society of London Series B - Biological Sciences 268 (1465): 413-422.

Wade, C. M., P. B. Mordan & F. Naggs. 2006. Evolutionary relationships among the pulmonate land snails and slugs (Pulmonata, Stylommatophora). Biological Journal of the Linnean Society 87 (4): 593-610.

I Gets Ejucated

This Sunday (i.e. the day after tomorrow) I'm heading to Adelaide to participate in the week-long National Postgraduate Training Workshop in Systematics that has been organised by the ABRS (Australian Biological Resources Study). This represents a quite welcome initiative and I personally hope that it becomes a regular occurrence - formal training in taxonomic methods is actually something of a rarity, and many of us (including yours truly) have had to essentially make a lot of it up as we go along.

As a result, I probably won't be posting anything for the next week - far too busy, darlings. See you all a week from Monday!

The Species-Scape Picture

This is probably one of the best demonstrations I've ever seen of the true diversity of organisms - in the picture above, representatives of various groups of organisms have been represented at sizes relative to the number of described species in that group. In case you're wondering where the mammals are, we're represented by the reindeer cowering underneath the mushroom.

I received this image from a work colleague - there are a couple of versions out there online that are obviously derived from the same source, but I don't know which is the original version. Contenders can be found at Cornell University and here.

Needless to say, this picture could change as our knowledge of the biosphere improves. The mammal and the bird are obviously too big, while the nematode and the fungus are two that I would expect to increase with time.

Update: Helen Schwencke has managed to establish that the first version of this image was by Quentin Wheeler and Frances Fawcett; see the comment thread below. Frances has supplied a copy of her original design:

My Name is LUCA

All workers on bacterial evolution dream that someday they may find LUCA. LUCA is the euphonious acronym for the Last Universal Common Ancestor, the theoretical organism or proto-organism from which all the living things we see around us today are descended. In a comment on an earlier post, though, I admitted to never being able to use the name LUCA without the tune to a certain 1987 Suzanne Vega hit running through my head*. Howard A. Landman agreed with me, and actually took it a little further. Without further ado, here are the lyrics he has penned for "My Name is LUCA":

My name is LUCA,
I lived on the ocean floor
near some hydrothermal vent
or maybe in a tidepool by the shore.
And everything that's now alive
is my descendant that survived.
All the others went away (x3)

I'm not the first life. No,
that was way before my time.
Things were so much simpler then,
the start of evolution's climb.
Born in a world of RNA,
or some say protein, some say clay.
No one knows just what it was (x3)

Now if you feel inclined
to explore your family tree,
you're gonna have a real hard time
tracing your way back down to me
'cause horizontal gene transfer
has left the path a tangled blur.
Still, it wouldn't hurt to try (x3)

(repeat first verse)

*The other option would be to channel the gnat from Alice Through the Looking-Glass and suggest a joke be made about "LUCA" and "lucre" - maybe "we all have one if not the other"?

Snails Letting It All Hang Out

This week's highlight taxon is the Scoliostomatidae, a distinctive small family of six genera of Devonian gastropods. For those unfamiliar with geological stratigraphy, the Devonian was Very Long Ago. It was during the Devonian that plants started making a real go of it in the terrestrial environment (they had arrived there earlier, but had so far been very half-hearted about the whole thing), while it wasn't until towards the end of the Devonian that some fishy thing gave thought to the possibility of investing in some piggly-wiggly toes. Of course, as marine organisms, Scoliostomatidae lived in an environment that had been long stocked with everything it needed and could have quite happily ignored the development of terrestrialised upstarts. The family is only known from what is called the "Old World Realm", the section of Devonian geography that incorporated what is now Australia, Asia, Europe, western North America, and the Morocco-India fringe of Gondwana (eastern North America was then part of the separate Appalachian realm). These were tropical seas at the time, and the Scoliostomatidae would have been warm-water taxa.

The Scoliostomatidae weren't recognised as a family until 2002, even though Scoliostoma itself had first been described as far back as 1838 (Frýda et al., 2002). Members of the family share a unique morphology - while most of the shell grows as a standard conical shape, the very last whorl of the shell undergoes a drastic change in direction, growing outwards and backwards (and in the case of four genera forming the subfamily Scoliostomatinae, upwards as well) from the rest of the shell. The image at the top of this post (from Frýda et al., 2002) shows Pseudomitchellia macqueeni, an inch-long member of the Mitchelliinae, the other two genera of Scoliostomatidae distinguished from the Scoliostomatinae in that the last coil did not have an upwards curve. In the left-hand photo in particular you can see how the aperture is facing in the wrong direction. This has the minor side-effect of making scoliostomatids buck the trend for the usual means of distinguishing dextral and sinistral gastropod shells - even though the aperture appears at first glance to be on the left-hand side, examining the rest of the shell demonstrates that it is actually on the right.

Though their distinctive morphology clearly unites the Scoliostomatidae as a group, the relationships of the family to other gastropods are completely unknown. This is sadly not unusual among Palaeozoic gastropods, especially such early forms as this. There was a time when gastropods were classified according to large-scale features of the shell, but study of Recent taxa has shown that such features are prone to significant homoplasy and are usually indicative of ecology rather than phylogeny. Instead, gastropod classification is more reliably based on such things as internal anatomy and the morphology of the protoconch, the larval shell which is visible as a small morphologically distinct region at the very tip of the adult shell. Internal anatomy is of course not preserved in fossils beyond possibly such basic points as muscle attachment scars. The protoconch is much more useful in studying fossil shells, but its small size and delicate nature means that it often fails to be preserved, and the chance of preservation becomes significantly reduced the older the fossil is (just to make things even more difficult, some gastropods shed the protoconch when they reach maturity). Many (if not most) Palaeozoic-only families are simply too old for more than a minuscule chance of protoconch preservation.

What was the ecological significance of the uncoiled scoliostomatid shell? In Recent gastropod families showing a loss of standard coiling, such as the worm-like Vermetidae and Siliquariidae, the uncoiled shell is related to a sessile filter-feeding lifestyle. Similarly uncoiled gastropods were even more widespread in the Palaeozoic than they were afterwards, or at least included representatives of a more diverse array of families. Indeed, a greater diversity of filter-feeders compared to today was a characteristic of Palaeozoic marine faunas in general, their disappearance generally attributed to an increase in predation pressure with the appearance of faster and more active predators. For Scoliostomatidae, the displaced aperture means that the bulk of the animal would have no longer been in line with the centre of gravity for the shell, meaning that they would have also had reduced motility and would have probably been fairly sedentary. However, in most filter-feeding uncoiled gastropods the uncoiled whorls became irregular in their growth. Scoliostomatidae retained a well-defined growth form with the aperture close to the remainder of the shell. The lifestyle of scoliostomatids remains unknown. I am going to speculate here that scoliostomatids may have been semi-sessile soft-sediment-feeders (if only because I like the sound of the phrase). If the aperture is directed downwards, then the remainder of the shell lies more or less flat on the substrate. The edge of the aperture would have also been more or less flush with the substrate, offering quite effective protection.

REFERENCES

Frýda, J., R. B. Blodgett & A. C. Lenz. 2002. New Early Devonian gastropods from the families Crassimarginatidae (new family) and Scoliostomatidae (new family), Royal Creek area, Yukon Territory, Canada. Journal of Paleontology 76 (2): 246-255.

The Ugly Stick in Action

Psettodes erumei, as depicted by Sir Francis Day.

I had two things I could have written about this morning, both of them very cool. There's the identification of possible chloroplast-derived genes in ciliates, for one. This is very neat, because ciliates belong to a group of protozoans called alveolates that also includes dinoflagellates. Dinoflagellates have red-alga-derived chloroplasts that contain chlorophyll c, a form of chlorophyll otherwise only found in chromists, the group of algae that includes brown algae and their unicellular relatives. On this basis, it has been suggested that chromists and alveolates together form a superclade called chromalveolates (as opposed, I suppose, to alveomists). See the post I wrote earlier about the discovery of the rather significant little alga Chromera velia for more details. Ciliates have been something of a fly in the ointment for this theory, as they contain nary a trace of a chloroplast, which might support the alternative idea that dinoflagellate and chromist chloroplasts are independently derived. Monophyly of chromalveolates would require that ciliates are derived from chloroplast-carrying ancestors that lost their ability to photosynthesise, something that chloroplast-derived genes in ciliates would make more credible.

The other option to write on was the identification of stem-flatfish. I was leaning towards ciliates, because the stem-flatfish story has already been covered by Ed Yong, GrrlScientist and Carl Zimmer, but I can't access the ciliate paper. So I guess that flatfish it is.

Flatfish are the group that includes such creatures as flounders, sole and halibut. Fish are, of course, the animals that invented ugly. With contenders such as gulper eels, sculpins and dories in action, the title of World's Ugliest Fish is hotly contended. While flatfish are far from being the winners at ugly (that position is quite firmly held by the anglers), they definitely deserve an Honourable Mention.


Flatfish larval development, from Pharyngula.

At some point in their history, both eyes of the ancestral flatfish moved onto the one side of their head. The eyeless side of the body is used by the fish to lie flat on the substrate (hence the name), so left and right have effectively become upper and lower (in most species, right is upper and left is lower, but there are some exceptions). The really odd thing is that flatfish actually hatch out as fairly normal-looking larvae, with the eyes in their usual places on either side of the body, and over the course of maturation one of the eyes migrates over the top of the animal to the other side. How this state of affairs came into being has been a difficult question, and Goldschmidt actually gave flatfish a significant role in his arguments for saltatory evolution (evolution happening by a series of rapid jumps), a theory that has been parodied as the "hopeful monster" position. A paper in today's Nature (Friedman, 2008) adds some crucial data to the debate, as well as confirming that the change took place gradually.

Friedman (2008) establishes that the fossil fish genera Amphistium and Heteronectes show distinctly asymmetrical eye positions on the skull. While the eyes are still on separate sides of the head, one eye is positioned distinctly higher than the other. That these were fully developed adult fish rather than larvae with eyes in the process of moving is indicated by the complete ossification of the skull. Phylogenetic analysis supports the position of the two genera as fossil outgroups to living flatfishes, lying along the stem. This position is supported by characters other than those related to the asymmetry of the skull, so is unlikely to represent convergence. Because the specimens lack distortion in other elements of the skull, Friedman was also able to conclude that the asymmetry was not the effect of post-mortem distortion.

The idea of a gradual development of flatfish asymmetry actually already had support from the living genus Psettodes, generally agreed to the sister taxon to other living flatfish. In Psettodes, the migrating eye moves to the other side, but only as far as just below the dorsal edge. It is also notable that Psettodes apparently spends more time swimming upright than other flatfish. While most flatfish species show a distinct developmental preference for which side the eye migrates to, with opposite-sided individuals as relatively rare mutations, Psettodes individuals may experience eye movement to either side during development. Interestingly, a study by Schreiber, 2006, on larval development in southern flounder (Paralichthys lethostigma) found that while all wild-caught specimens were left-sided, 16% of larvae in the lab developed right-handedly, while 4% of larvae actually developed bilaterally symmetrically, with either the eyes remaining where they were or both moving dorsally. It seems likely that the failure to find such variants in the wild indicates that for some reason or other they do not generally live to adulthood.


From Friedman (2008).

Of course, the identification of these asymmetrical ancestral forms still leaves a lot of questions open. What we still don't know, of course, is why the ancestors of flatfish started lying on their sides, and why they became asymmetrical. The asymmetrical-but-not-one-sided forms Amphistium and Heteronectes are known from two stages of the Eocene, and were contemporary with more derived crown flatfishes, so they were not a short-lived maladaptive form that shuffled off as soon as their better-adapted descendants arrived. It has been suggested that the flattened habitus of flatfishes allows them to better conceal themselves while waiting for other fish as prey, which they are then able to ambush from below, and Amphistium, like living flatfish, does appear to be piscivorous. Side-resting fish may have been subject to selective pressure for eye asymmetry that allowed them to keep an eye out for prey while remaining concealed, and Friedman suggests (in comparison with modern flatfish behaviour) that Amphistium and Heteronectes may have been able to prop themselves up on their pectoral fins, raising the lower eye above the substrate and allowing them to 'squint' for prey. At the moment, of course, this is all speculative. From the aforementioned developmental studies (Schreiber, 2006), though, we can add some details. As well as having the eyes move sides, the larvae also change from swimming vertically to swimming laterally, but the two are independent events. Change in swimming orientation occurs before eye migration, and that small percentage of larvae that did not experience eye migration still changed swimming orientation. In a very small fraction of larvae, swimming orientation actually developed in the opposite direction to eye migration, so they ended up swimming with the eyes on the underside (needless to say, these unfortunate individuals did not live long). Further investigation of how asymmetry develops in living flatfishes - particularly the basal Psettodes - may shed further light on how this remarkable condition arose in the first place.

REFERENCES

Friedman, M. 2008. The evolutionary origin of flatfish asymmetry. Nature 454: 209-212.

Schreiber, A. M. 2006. Asymmetric craniofacial remodeling and lateralized behavior in larval flatfish. Journal of Experimental Biology 209: 610-621.

Linnaeus' Legacy #9: Classifying the Classifiers

The latest edition of Linnaeus' Legacy (binomial) is up at Biological Ramblings. This month's keywords: foraging niche; essential foundation; butterflies and moths; scorpions of Kenya; prejudices, errors, and difficulties; too much work; human bias; silly myth; Antarctosaurus; children's perceptions; all 130 of them; golden age of discovery; already extinct; beaked whales; things are getting wierd; you can never have enough nudibranchs; supermajors; baleen whales; urban island; broadbill; species richness in bacteria; no unique rank.

Of Lions and Lace

The "non-green, green lacewing" (Catanach, 2007) Abachrysa eureka. Photo by M. C. Thomas.

There is a term that bird-spotters use to describe the ability to recognise what species a bird belongs to even if one cannot see the details of its features - they refer to the "jizz" of a bird, derived from the acronym GIS for "general impression and shape". The jizz of a bird species is not something that can be described easily, if at all - it is something that can really only be appreciated with experience. It should hardly come as a surprise that the same concept applies with identifying other organisms just as much as birds. Lacewings (Neuroptera) are a smallish order of insects (only about 5000 species) that include a diversity of forms, but many look at first glance not unlike small dragonflies. Still, a closer look will reveal significant differences to a dragonfly. For a start, lacewings have longer antennae and are able to fold their wings back over their abdomen in a way that no dragonfly can. There is also the feature that gives them their name - the wings of lacewings are particularly densely covered with veins, the little criss-crossing fluid-carrying lines that you can see on any insect wing. While you might need to look very closely indeed to see the individual veins, the cumulative effect of the dense veins is to give lacewing wings a distinctive shimmer, like light off satin, or the glimmer of colour across oil. This week's highlight taxon is a specific group of lacewings - the tribe Belonopterygini.

Lacewings have a complete metamorphosis, meaning they have a distinct larval stage separated by a dormant pupal stage from a very different-looking adult. Most lacewings start out life as formidable predators, and are quite recognisable by their large, protruding jaws. The most famous are the antlions of the family Myrmeleontidae, which dig themselves conical pits at the bottom of which they lie dug into the soil, waiting for any small insects unlucky enough to fall into the pit. While the large jaws are used for capturing and macerating prey, lacewing larvae are actually liquid feeders, injecting digestive saliva into their prey then sucking out the dissolved juices (Canard, 2007). One intriguing (yet kind of disgusting) feature of the order is that the midgut is not actually connected to the hindgut until pupation, meaning that the larva is not capable of defecation. Any indigestible waste products are stored in the gut until the lacewing reaches adulthood and passed after emerging from the pupa. Can you imagine the relief?


The belonopterygin Italochrysa insignis. This photo illustrates very well the distinctive shimmer that neuropteran wings possess in the right light and which I've found is actually one of the quickest ways to recognise an adult lacewing. Photo by Sheila.

Belonopterygini are a cosmopolitan tribe of a different family, the Chrysopidae (green lacewings), whose larvae are active hunters, many of them of economic significance as predators of plant pests such as aphids and thrips. Belonopterygin larvae are specialist associates of ant nests (Freitas & Penny, 2001), feeding on the ants therein. Unfortunately, such specialist habits make Belonopterygini one of the less-studied chrysopid groups, and I have been unable to find how the larvae evade detection by the ants. Like other chrysopids, belonopterygin larvae use small bits of soil and debris to disguise themselves, starting with the shell of the egg they hatched from (Catanach, 2007). Larvae of other chrysopids have been observed to incorporate the husks of drained prey into their trashy disguises so I would be interested to know if belonopterygins do the same, as has been described recently for assassin bugs.

Adult chrysopids may be predacious like the larvae, or they may feed on non-live food such as honeydew. Honeydew-feeding species possess diverticula in the gut that house symbiotic yeasts aiding the lacewing in digestion. Sounds produced by tapping the abdomen on the substrate are used by chrysopids in courtship, and the pattern of sounds produced may differ significantly between closely related species (New, 1991). Eggs are laid perched on the end of long silk threads.

REFERENCES

Canard, M. 2007. Natural food and feeding habits of lacewings. In Lacewings in the Crop Environment (P. McEwen, T. R. New & A. Whittington, eds.) pp. 116-129. Cambridge University Press.

Catanach, T. A. 2007. Abachrysa eureka (Banks) (Neuroptera: Chrysopidae): egg, first instar larva and biological notes. Unpublished thesis, Texas A & M University.

Freitas, S. de, & N. D. Penny. 2001. The green lacewings (Neuroptera: Chrysopidae) of Brazilian agro-ecosystems. Proceedings of the California Academy of Sciences 52: 245-395.

New, T. R. 1991. Neuroptera. In The Insects of Australia (CSIRO, ed.) pp. 525-542. Melbourne University Press.

The Origins of Flowers

Reconstruction of the bennettitalean Williamsonia, a potential stem-angiosperm. Image from Turbo Squid.

I'm going to break one of the supposed blogging rules - I'm going to feed a troll. In the comments thread to the bird evolution post I wrote recently, one commenter brought up the supposedly intractable evolutionary problem of the "sudden" appearance of flowering plants. I briefly responded to this comment at the time, but I thought the question is an interesting enough one to deserve further investigation. So here is my presentation on why the "sudden" appearance of flowers was not so sudden.

The origin of the angiosperms (flowering plants) has long been considered one of the great unsolved questions of biology, and I must confess to having occassionally slipped into the hyperbole myself. However, we actually have some much better ground to stand on than the hyperbole might suggest.

First off, we need to ask what exactly makes flowering plants so distinct? What do they have that no other plant has? I bet some of you are fighting the urge to reply with, "They have flowers. Duh." To which I have to reply - wrong! After all, you could debate to what extent the reproductive structures of many flowering plants can really be called 'flowers'. Many flowering plants lack the petals and/or sepals of more classic flowers. They may have bracts (coloured leaves) instead, like poinsettias or bougainvilleas, while many wind-pollinated angiosperms simply do without ornamentation entirely. And if we argue that petals are not necessary to count as a flower - if those plants that surround their reproductive structures with bracts also count as having flowers - then flowers are not actually unique to angiosperms (as I'll explain in a minute). No, the really significant feature of angiosperms is the carpel, the protective covering of two integuments that encloses the ovule of angiosperms. In other living seed plants, the gymnosperms, the ovules generally have only one integument and are produced exposed on the ends of short branches, often surrounded by a protective whorl of leaves or leaf-derived structures to form a structure called a strobilus (in many conifer groups, these protective leaves have become hard and woody to form the scales of a cone with an ovule at the base of each scale). Morphological and molecular phylogenetic analyses disagree significantly about the relationships between angiosperms and living gymnosperms (Friedman & Floyd, 2001). Morphological analyses place angiosperms nested within gymnosperms, forming a clade with the Gnetales, while molecular analyses place the angiosperms as sister to all living gymnosperms, not closely related to Gnetales.

While there is a significant divide between the carpel-enclosed ovules of angiosperms and the exposed ovules of gymnosperms in living taxa, this divide (unsurprisingly) actually dwindles when we consider fossil taxa. Debate still rages about which fossil taxa are the closest relatives of angiosperms, but two taxa that pop up on a regular basis are the Bennettitales and Caytonia. These taxa are often closely related to angiosperms and the Gnetales in morphological analyses (Doyle, 1998), while if morphological analyses are constrained to match the molecular trees the angiosperms form a clade with Bennettitales, Caytonia and glossopterids (Doyle, 2006). The Bennettitales and Caytonia both put in an appearance during the Triassic and survived until the end of the Cretaceous, while angiosperms are first known from the early Cretaceous (Doyle, 1998). Caytonia is generally described as a "seed fern", which were usually trees, but articulated fossils are fairly rare. It produced multiple single-integument ovules reflexed and contained within a protective structure called a cupule. It does not take a significant leap to imagine the reduction to a single ovule per cupule and the cupule developing into the outer integument of the angiosperm carpel.


(From Frohlich & Chase, 2007) Reproductive structures of fossil stem-angiosperm candidates. a, Glossopteris showing cupules borne on stalk above a leaf. b, Caytonia male (above) and female (below) reproductive units. c, Caytonia cupule. d, Corystosperm (Umkomasia) cupule containing one ovule. Cupule wall almost surrounds ovule, except for a slit facing the stalk. e, Bennettitales (Williamsoniella) bisexual reproductive unit; each oval pollen sac consists of several fused microsporangia. Ovules are borne among scales on the central stalk; in Vardekloftia each is enclosed by a cupule wall. Green, cupule wall; red, ovule; yellow, pollen organ.

Bennettitales were plants fairly similar in appearance to modern cycads that lacked any such carpel-like arrangement and had ovules born along scales in the strobilus. What Bennettitales did have, however, were flowers (of a sort). The leaves of the strobilus were expanded into flower-like bracts that were quite large (and possibly quite colourful) in a number of taxa. Certain features of the bennettitalean bracts suggest that they had a role in attracting insect pollinators, just as modern flowers do today (Gottsberger, 1988). The largest bennettitalean "flowers" were found in Cycadeoidea, which had the bracts recurved to enclose a central chamber containing the reproductive organs. This is of great significance because similar arrangements are found in modern beetle-pollinated flowers, which are believed to be among the more basal flower forms. Also significant is the presence in bennettitalean fossils of the chemical oleanane, derived from a secondary metabolite that is only produced by angiosperms among living taxa, further supporting their relationship (Taylor et al., 2006).

The earliest major pollinators of flowers were probably beetles and flies (Kevan & Baker, 1983). Beetles in particular are the major pollinators of members of basal angiosperm orders such as Magnoliales and Nymphaeales. The two insect groups most commonly associated with pollination in most peoples minds, butterflies and bees, were unlikely to have been significant players in the origin of flowers for the simple reason that neither had come into existence yet - Lepidoptera as a whole only started making an appearance during the Cretaceous, while bees were not to appear until the Tertiary. As already noted, many of the basal angiosperm groups show adaptations towards beetle pollination (this is why magnolias, for instance, produce such a powerful perfume and white flowers - nocturnal beetles use smell more in finding food, while white stands out more at night than colour would). Many beetle-pollinated flowers have some sort of enclosed chamber, or close during the day, providing their pollinators with a safe haven from predators as well as providing food in the form of nectar or pollen (it is quite alright if the pollinator eats some of the pollen so long as the flower produces far more than the pollinator can eat - indeed, if the pollinator is actually going for the pollen then it will almost certainly be rooting around in it and getting covered with it), and this may have been the approach Cyacadeoidea was going for. On the other hand, another basal angiosperm family, the Winteraceae, have open and unspecialised flowers that attract a wide range of pollinators such as beetles, moths, flies and thrips.


Arabidopsis with induced mutation causing leaves to be partially converted into petals. Photo from University of California, San Diego.

Insect-attracting strobili such as found in Bennettitales could have quite easily given rise to the first flowers. Developmental genetics has confirmed the theory put forward many years previously that petals and sepals represent modified leaves, and by affecting the expression of the genes involved it has proved possible to make leaves grow instead of petals, and petals grow instead of leaves (Goto et al., 2001). So while we have still not entirely solved what Darwin so overquotedly referred to as the "abominable mystery", the answer has drawn tantalisingly close.

REFERENCES

Doyle, J. A. 1998. Molecules, morphology, fossils, and the relationship of angiosperms and Gnetales. Molecular Phylogenetics and Evolution 9 (3): 448-462.

Doyle, J. A. 2006. Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133 (1): 169-209.

Friedman, W. E., & S. K. Floyd. 2001. Perspective: The origin of flowering plants and their reproductive biology - a tale of two phylogenies. Evolution 55(2): 217-231.

Frohlich, M. W., & M. W. Chase. 2007. After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450: 1184-1189.

Goto, K., J. Kyozuka & J. L. Bowman. 2001. Turning floral organs into leaves, leaves into floral organs. Current Opinion in Genetics and Development 11 (4): 449-456.

Gottsberger, G. 1988. The reproductive biology of primitive angiosperms. Taxon 37 (3): 630-643.

Kevan, P. G., & H. G. Baker. 1983. Insects as flower visitors and pollinators. Annual Review of Entomology 28: 407-453.

Taylor, D. W., H. Li, J. Dahl, F. J. Fago, D. Zinniker & J. M. Moldowan. 2003. Biogeochemical evidence for the presence of the angiosperm molecular fossil oleanane in Paleozoic and Mesozoic non-angiospermous fossils. Paleobiology 32: 179-190.

The 150th Anniversary

As reported by Aydin Örstan, it was 150 years ago today that the theory of natural selection of Charles Darwin and Alfred Wallace was presented to a meeting of the Linnean Society. Neither Darwin nor Wallace was present when it happened - Darwin's 19-month old son had died from scarlet fever only a few days earlier, while Wallace was still in Malaysia. Instead, the three letters (two by Darwin and one by Wallace) were presented in their place by Charles Lyell and Joseph Hooker, the latter having withdrawn one of his own papers in order to present the letters. The presentation seems to have been something of a non-event - while Joseph Hooker was many years later to recollect that the scholars attending the meeting sat stunned by the import of what they were hearing, it seems more likely from the dearth of responses closer to the time that they were merely worn out after a long and busy meeting. Darwin himself was to later record that, "Nevertheless, our joint productions excited very little attention, and the only published notice of them which I can remember was by Professor Haughton of Dublin, whose verdict was that all that was new in them was false, and what was true was old." Like so many significant events, its importance was not to be recognised until later.

REFERENCES

Moody, J. W. T. 1971. The reading of the Darwin and Wallace papers: an historical "non-event". J. Soc. Biblphy nat. Hist. 5 (6): 474-476.

Carnival Time!

Doug Taron has the new Circus of the Spineless up at Gossamer Tapestry. There's a heavy emphasis on insects this time around, but then, there's a heavy emphasis on insects around the planet in general.

And while we're on the subject of carnivals, it's time to get your submissions in for Linnaeus' Legacy! This month's edition will be being hosted by Nick Sly at Biological Ramblings (assuming, of course, that he doesn't get eaten by monitors between now and then), so get your submissions into me, him, or use the handy BlogCarnival submission form!