Thursday, September 17, 2015

Is there a Gasterosteologist in the house? That is, someone to help us understand the Three-Spined Stickleback, Gasterosteus aculeatus Linneaus 1758 by Don Orth

The Three-Spined Stickleback is the only Stickleback that occurs in Virginia and furthermore, it is also the most widespread Stickleback in the world.    It’s name Gasterosteus is derived from the Greek words (gastro and osteo) that literally translate to “belly” “made of bone,” while aculeatus means “spiny.”  I believe that each fish has something to teach us, if we just observe closely and ask the right questions.  However, the Three-Spined Stickleback has so much to teach us.   In fact, in today’s library search on  “Three-Spined Stickleback Gasterosteus aculeatus” I learned that there are 5,267 journal articles, 1,042 books, and 336 doctoral dissertations written on this species alone!  In this short post, I will briefly describe many of the lessons the species can teach us.   How to be a fantastic Dad?  How to teach kids self defense?  How to be a good househusband?   How to court the ladies? How to keep embryos well oxygenated?  How to wear red to attract a mate? How to cooperate with others to avoid predators? How to see all four major wavelengths of light including ultra-violet?

Three-Spined Stickleback Photo by by Lubomir Hlasek
The Three-Spined Stickleback is easy to identify by its laterally compressed body with a very slender caudal peduncle, large terminal mouth, large eye, and three spines anterior to a soft-rayed dorsal fin.   It has no scales on the body; instead it has bony plates on its back, flanks, and belly.   The number of plates on its flanks varies widely across its range and that is another story worth telling.    The pelvic fin is unique as it is made up of only a single spine.   Dorsal colors are drab olive or a silvery green, sometimes with brown or black mottling.  Flanks and belly are silvery.  During breeding, the eyes of males become blue and the lower head, throat, and anterior belly turn bright red.    Do the Sticklebacks reflect the origin of a human preference for a blue-eyed mates?   

The Three-Spined Stickleback inhabits fresh, brackish, or salt water along coasts of North America, Europe, and northern Asia.  There are both freshwater and anadromous forms.   Freshwater forms exist in waters with connections (current or past) to the coasts.   In Virginia, it occurs in the York and James basins and tributaries of the eastern shore.   The anadromous form spends most of its life in the sea, and returns to freshwater to breed.   This form shows less geographic variation in number of lateral bony plates (usually 30-40) and has long dorsal and pelvic spines.   Freshwater forms of the Three-Spined Stickleback have larger variation in bony armor and shorter dorsal and pelvic spines.     Apparently, since the end of the last ice age, Three-Spined Sticklebacks have repeatedly colonized new streams and lakes forming unique populations. 

Because it is a small fish, there are many predators including fish, birds, and even dragonflies.  Predation pressure is a strong selective pressure on the species and is reflected in the variation in size and number of bony armor plates and size of spines.    These anti-predator defense mechanisms have been widely studied.  
Photo by Marcin Lenart
Photo by David Moreton
In fact the difference in the bony skeletal patterns of closely-related populations of Three-Spined Sticklebacks reflects a difference in a single gene.  This gene is called a “tool-kit” gene because it possesses all the tools to program all processes involved in bone formation.  Interestingly, two forms of the Three-Spined Stickleback, which differ in the size of their pelvic fins, have repeatedly evolved in freshwater lakes.    Mike Shapiro and David Kingsley showed that long pelvic spines protect the open-water form from attack by other fish. Yet in the bottom-dwelling form (lower image), whose principal predator is dragonfly larvae rather than other fish, the tool-kit gene controlling the formation of the pelvic fin has been selectively turned off.
    Two forms of Three-Spined Sticklebacks.  The bony plates in are shown in red.  
from David Kingsley, modified from Cuvier (1829)  

The love life of the Three-Spined Stickleback is complicated to say the least. The male Three-Spined Stickleback  first digs a pit and begins to assemble nest materials from algae and vegetation.   During the nest builder phase he has inconspicuous colors.  The nest materials are glued together with spider-web-like threads in a spherical shape with a tunnel for he and his mate to enter.   The “glue” is called spiggin (the Swedish name for Stickleback), which is a proteinaceous substance secreted from the kidney.    In more than a few experiments on nest-construction, the male Stickleback demonstrated a preference for brightly colored nest materials to decorate the nest entrance.   After the nest is constructed, the male develops a bright red throat, which is a sign that he is ready to breed.   When the male develops bright colors he becomes very aggressive and defends his territory from other males. 

Photo of Three-Spined Stickleback gluing materials in nest.

The breeding male will attack anything with red color that gets near its territory.  This is called a fixed action pattern in ethology to denote an “instinctive behavioral sequence that is relatively invariant within the species and almost inevitably runs to completion.”     Ethologist Nikolass Tinbergen first described this automatic behavior in sticklebacks and also witnessed sticklebacks attacking red mail trucks they observed through the glass aquarium walls and windows.  The fixed action pattern has a proximate explanation --  the red color causes the male to respond aggressively.   The ultimate explanation is that the male behavior decreases the chance that eggs laid in his nesting territory will be fertilized by another male.

Close up of male Three-Spined Stickleback with nuptial coloration. Photo (c) Ecomare.
Females are courted and encouraged to deposit eggs in that nest, but that courtship too is complicated.     In order to successfully court a female, the male must demonstrate traits of the superb, hypervigilant house-husband.     The male performs a courtship ritual  to entice females to lay their eggs.    This includes a dance (or swim) that has been named the “zigzag” dance.  The male approaches with a zigzag dance, bites the female, and then swims to the nest site with the same zigzag dance.   The male hopes the female follows him to the nest. 
Nuptial male Three-Spined Stickleback biting potential mate.
The female selects a mate based on red throat color and other visual signals, such as the nest decorations.  The red nuptial coloration is clearly a cue to females as experiments have shown that ripe females were more likely to follow a “dummy” stickleback to a fake nest if the dummy had a red belly.    Further, dominant males express redder colors than subordinates.  Maybe she is also attracted to his intense blue eyes – though this hypothesis has not been tested.  But there is more to the reproductive behavior than color variations.  Remember, the love life of the Three-Spined Stickleback is complicated.   The male may receive eggs from more than one female but all parental care is  provided by the male. 

After the female lays her eggs and leaves the nest, the male changes from sexual phase to a parental phase and his color again becomes dull and cryptic.  These changes are associated with a dramatic drop in plasma testosterone levels.     The parental (low testosterone, dull color) phase includes parental duties, guarding the fertilized eggs, fanning them with his pectoral fin and/or tail to provide them with oxygen, and protecting eggs from predators.    The parental phase may last 5-10 days until the eggs hatch and the phase is energetically very costly.

Because of these costs associated with being the perfect house-husband, the Three-Spined Stickleback male may engage in other “bad” behaviors to more easily pass on genes.  These bad behaviors include nest raiding to steal fertilizations in other nests, stealing eggs from other nests, and eating eggs from other nests.

Another lesson learned from numerous studies of the Three-Spined Stickleback is the potential for rapid speciation.  This is often apparent in the existence of closely associated species pairs.   In Paxton Lake, Texada Island, southwestern British Columbia, two distinct sympatric forms were derived after glacial retreat.  Anadromous Three-Spined Stickleback repopulated lakes after poisoning and rapidly adapted to the new environment through natural selection.  For more information, view this video.  

Limnetic male (top left) and female (top right) and benthic male (bottom left) and female mature (bottom right) sticklebacks. The limnetics are about 65 mm total length and the Benthics about 75 mm. Photo by G. Velema, UBC

Recently biologists discovered ultraviolet (UV) receptors in the eyes of some fishes, including the Three-Spined Stickleback.   The nuptially colored male reflects UV radiation from parts of his body and this may permit short-range communication between male and potential mates. 
One of the anti-predation strategies used by Three-Spined Sticklebacks is cooperation (tit for tat) in keeping a watch on potential predators.   In this behavior pairs of sticklebacks reciprocate as each takes turns watching for predators. 

The Three Spined Sticklebacks teach us that evolution is occurring on a timescale much faster than we might imagine.   For example, marine and freshwater forms are maintained in downstream and upstream locations with extensive hybridization at intermediate sites.   We can expect future studies that take advantage of recent sequencing of the entire genome (Jones et al. 2012) allowing further study of the molecular basis for evolution of this species.


Jones et al. 2012. The genomic basis of adaptive evolution in threespine sticklebacks.  Nature 484:55-61.   doi:10.1038/nature10944

Ostlund-Nilsson, S., I. Mayer, and F.A. Huntingford, Editors.  2006. Biology of the Three-Spined Stickleback.  CRC Press.   408 pp.

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