Pregnant males

...are the rule in seahorses, and non-existent in all other vertebrates.

I had intended, in this week’s post, to discuss several new papers out this week. There’s one on how in house sparrows, eating a diet that is out of whack makes birds slower to learn, quicker to anger, and generally more stressed. And another on social connections in giraffes, claiming to find—wait for it—that male and female giraffes are…different. But I don’t yet have access to the full text of either of those articles, which means I’m not yet in a position to comment.

One paper that came out this week which I do have access to is about seahorses, so I’m going to focus there.

The scientific family Syngnathidae includes more than 200 species of seahorses, seadragons, and pipefish; for the purposes of this post I will refer to them collectively as seahorses. They are fish—not in the “yes well sparrows and giraffes and humans are fish so of course they too are fish” sense (which is true, a point I will return to in another post, but for now, if you’re interested, see this excellent piece from Bret from a few years back, On Being A Fish, or check out chapter 2 of A Hunter-Gatherer’s Guide to the 21st Century). Rather, seahorses are ray-finned fish—Actinopterygians for the Latin or phylogenetically inclined. The ray-finned fish include pretty much everything that you think of when you think of fish: tuna and trout, salmon and sunfish, clownfish and carp. (But not sharks or lungfish, for different reasons, on which, again, more another day.)

Seahorses are not easily mistaken for anything else in the sea, but most people don’t realize just how unique they are. A 2019 paper on feeding morphology in this clade describes them as “a family of marine predators that ambush small prey items in complex habitats.” This is a description that I enjoy, if largely because when I consider seahorses, “marine predator” is not the first thing that comes to mind. But predators they are, and they accomplish their predation by a mechanism known as “pivot feeding,” by which they propel their mouths, attached to those signature snouts, extremely rapidly towards prey, using elastic recoil of post-cranial tendons (this is yet another remarkable scientific rabbit hole to go down which, if you’re interested, click on either link in this paragraph and you’ll be off to the races).

The aspect of seahorse biology that most people will be more familiar with is that males do all of the parental care: rather than maternal or bi-parental care, seahorses exhibit paternal care. That in and of itself is rare, but not that rare, especially among ray-finned fishes. Lots of ray-finned fishes have paternal care. But the particular way that seahorse males engage in paternal care is incredibly rare: they brood their young on board their own bodies, in a fashion reminiscent of the female pregnancy of all mammals save but a few weirdos at the base of the mammalian tree—the duck-billed platypus and the echidnas.

During seahorse sex, the female transfers unfertilized eggs to the male’s brood pouch. Only then, after receiving them into his own body, does the male fertilize the eggs, after which he carries and nurtures his embryos for several weeks in his brood pouch, before finally giving birth to live young.

This is all very, very unusual. Indeed, among vertebrates, seahorses are the only species in which males exhibit pregnancy. (Yet another fascinating biological story to track is how young are produced into the world—via egg (oviparity), via live birth (viviparity), or via a hybrid mode known as ovoviviparity. I have made far too many promises of this sort in this week’s post, but: to this I will also return another day.)

So, given viviparity (live birth) in seahorses, the only vertebrate clade in which males do the brooding, how do they pull it off? Enter this week’s new research by Dudley at al, a team of Australian scientists.

This new paper summarizes the great diversity of “embryo attachment types” across seahorse species—a finding paralleled, incidentally, by the great diversity of placentas found across mammalian species. Dudley et al then focus on some of the most complex of brood pouches out there, those in the genus Hippocampus. Not only, in these seahorses, does the expression of many types of genes change in the placental tissue during male pregnancy, but, the new research finds, the tissues themselves change dramatically, becoming thicker and more diffuse as they enclose the developing embryos. The authors conclude that “the structural similarities between male pregnancy in seahorses and female pregnancy in other vertebrates support the assertion that common physiological challenges of internal embryo incubation have led to convergent adaptations in live-bearing species.”

The concept of convergence is a powerful one. Truly independent solutions to problems that distantly related organisms are experiencing are said to be convergently evolved. When considering what it means for something to be “the same,” we need to ask, at least in evolution-space: Is it the same due to common ancestry (homology), or due to similar problem-solving from disparate starting blocks (homoplasy, or convergence)? Is the flight of dragonflies, swans, and bats homologous or convergent? How about the flight of swans, swallows, and sandpipers?

The Most Recent Common Ancestor (MRCA) of dragonflies, swans and bats did not fly—that animal was very basal, relatively simple, and certainly without flight. So the flight of those three organisms is convergent. At least three times in those three lineages, flight evolved. But the Most Recent Common Ancestor of swans, swallows and sandpipers was itself a bird—and had flight.  Therefore the flight of these three organisms—birds, all—is homologous. Flight evolved once and only once in their shared lineage. Their similarities—in this case, their flight—is due to shared ancestry. The similarity, in the case of flight between different species of birds, is truly about it being the same thing.

All of which leaves unaddressed perhaps the most interesting thing about male pregnancy in seahorses: Why do they do it? What unusual environmental conditions provided the selective pressure to keep females out of the parental care game in this clade, while pushing males into a set of anatomical, physiological and behavioral spaces into which males otherwise do not go?

The short answer is: the seahorses are so diverse, and only a very few species very well known, such that we do not yet have enough information to answer the question.

One thing that we can say is this: “male pregnancy” would seem to be the epitome of sex-role reversal. In species as varied as elk and peacocks, elaborate male displays are both a form of courtship to attract females, and a competitive signal to warn other males to keep away. In many species of seahorses, in contrast, it is the females who tend to have elaborate courtship displays, in the form of bright colors, or aggressive behavior. It is also true, however, that in some seahorse species males also have displays that appear to attract mates: yellow noses, or swollen brood pouches, or fancy stripes. Thus, while there is ample evidence of females taking on male-typical behaviors in seahorses, there is also evidence of males continuing to do what males typically do—with the additional fact of them also being the ones to gestate the young.

So: male seahorses gestate their young, but most of them are not exactly sex-role reversed. Many of them, in fact, are monogamous, which reduces the extremity of sexually selected characters in both sexes: both sexes will be expected to compete for mates, and both sexes are expected to engage in courtship, and be choosy about with whom they mate. Seahorses are thus sex-role reversed in some regards, but not completely, and not really. There’s another species that fits that description: humans. More on that another time.

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