Placoderm double penis: not the primitive trait they think it is

Summary, for those in a hurry:
Contra the title of this Long et al. 2014 paper, the presence of bony claspers (shark-like dual lateral penises) does not signal the origin of gnathostome internal fertilization on this tiny, jawless placoderm, Microbrachius (Fig. 1). Contra Long et al., internal fertilization never gave rise to external fertilization in gnathostomes. Long et al. added Microbrachius to a cladogram invalidated by the exclusion of extant taxa (Fig. 2).

Massive taxon exclusion
in Long et al. 2014 recovered an incomplete and invalid cladogram (Fig. 2) that mistakenly (yet traditionally) nested placoderms with osteostracans and spiny sharks with sharks by excluding all extant taxa and several pertinent extinct taxa.

By contrast
the large reptile tree
(LRT, 1744+ taxa, subset Fig. 3), minimizes taxon exclusion and separates all four clades. In both cladograms (Figs. 2–4) claspers and internal fertilization are phylogenetically separated and thus arose at least twice by convergence in sharks and placoderms.

Figure 1. Microbrachius dicki female and male (with dual lateral penis) specimens several times larger than life size.

Figure 1. Microbrachius dicki female and male (with dual lateral penis) specimens several times larger than life size.

From the Long et al. 2014 abstract
“Reproduction in jawed vertebrates (gnathostomes) involves either external or internal fertilization1. It is commonly argued that internal fertilization can evolve from external, but not the reverse. Male copulatory claspers are present in certain placoderms, fossil jawed vertebrates retrieved as a paraphyletic segment of the gnathostome stem group in recent studies.”

This is incorrect, according to the LRT (subset Fig. 3). A valid phylogenetic context is missing in Long et al. 2014 (Fig. 2) largely due to excluding extant taxa. In Long et al. 2014 Microbrachius is a basal placoderm, basal to sharks and bony fish. By contrast, in the LRT Microbrachius is a derived taxon, a sister to Bothriolepis, leaving no descendants.

Figure 2. Cladogram from Long et al. 2014 lacking any extant taxa and suffering from massive taxon exclusion relative to the LRT in figure 4.

Figure 2. Cladogram from Long et al. 2014 lacking any extant taxa and suffering from massive taxon exclusion relative to the LRT in figure 4.

The Long et al. 2014 abstract continues:
“This suggests that internal fertilization could be primitive for gnathostomes, but such a conclusion depends on demonstrating that copulation was not just a specialized feature of certain placoderm subgroups.”

This is incorrect. According to the LRT sturgeons (Pseudoscaphirhynchus) are pre-gnathostomes and they produce millions of eggs through external fertilization. Paddlefish (Polyodon) are basal gnathostomes and they produce hundreds of thousands of eggs through external fertilization. Between them the Chondrosteus clade includes whale sharks (Rhincodon) and manta rays (Manta) and those two produce only a few young with live birth after internal fertilization. In the same clade, Loganellia (Early Silurian) is the earliest known fossil gnathostome and its reproductive strategy remains unknown at present.

Figure x. Subset of the LRT focusing on fish.

Figure 3. Subset of the LRT focusing on fish. Here, by including extant taxa, sharks are not related to spiny sharks and placoderms are not related to jawless fish.

The Long et al. 2014 abstract continues:
“The reproductive biology of antiarchs, consistently identified as the least crownward placoderms and thus of great interest in this context, has until now remained unknown.”

The addition of fish to the LRT postdates the publication of Long et al. 2015, so the authors did not realize their cladogram became erroneous by excluding extant taxa. After adding taxa (in the LRT) antiarchs are bottom-dwelling placoderms that reduce or lack mandibles as a derived, not a primitive condition.

The Long et al. 2014 abstract continues:
“Here we show that certain antiarchs [placoderms] possessed dermal claspers in the males, while females bore paired dermal plates inferred to have facilitated copulation. These structures are not associated with pelvic fins. The clasper morphology resembles that of ptyctodonts, a more crownward placoderm group, suggesting that all placoderm claspers are homologous and that internal fertilization characterized all placoderms.”

In the LRT ptyctodonts (like Campbelllodus) are closer to catfish (like Clarias) rather than the rest of the traditional placoderms.

In their efforts to simply illustrate their hypothesis,
the cladogram diagram in Long et al. 2014 (Fig. 4) cherry-picked taxa and “Pulled a Larry Martin” by focusing on copulatory organs to the exclusion of a suite of other traits. Excluding all extant taxa is the main problem with this paper. The LRT includes extant taxa and falsifies the cladograms of Long et al. 2014 (Figs. 2, 4) restricted to a select list of extinct taxa, that was the traditional list until the LRT expanded to include fish.

Figure 4. Cladogram diagram from Long et al. 2014 cherry-picking taxa and concentrating on one trait while ignoring extant taxa.

Figure 4. Cladogram diagram from Long et al. 2014 cherry-picking taxa and concentrating on one trait while ignoring extant taxa.

The Long et al. 2014 abstract continues:
“This implies that external fertilization and spawning, which characterize most extant aquatic gnathostomes, must be derived from internal fertilization, even though this transformation has been thought implausible.”

No. That conclusion arises from a phylogeny invalidated by taxon exclusion. In the LRT, by minimizing taxon exclusion the transformation from internal to external fertilization is not documented. External fertilization is always more primitive. Internal fertilization occurred by convergence several times in vertebrate phylogeny.

Just so you know…

  • Sea lampreys produce 30 thousand to 100 thousand eggs
  • Sturgeons produce 100 thousand to 3 million eggs
  • Manta rays give birth to 1.5m babies
  • Whale sharks give birth to .5m babies
  • Paddlefish produce 70 thousand to 300 thousand eggs
  • Moray eels produce 10 thousand eggs
  • Catfish produce 4 thousand to 100 thousand eggs
  • Coelacanths give birth to 5 babies
  • Basal tetrapods, like frogs and salamanders, produce dozens of eggs

Long J Mark-Kurik E, Johanson Z et al. 2014. Copulation in antiarch placoderms and the origin of gnathostome internal fertilization. Nature 517, 196–199 (2015).



The origin and evolution of sex organs in mammals

Yesterday we looked at the origin and evolution of the human face.

Today we hit below the belt
We’re going for the gonads. If you’ve ever wondered the ins and outs of where, how and why your privates arose, this is your primer.

This topic also comes under the subject of reptile evolution because mammals are reptiles, according to the large reptile tree. This is heresy, of course, bucking decades of tradition. However, now the amniote/reptile tree has a new topology simply by adding taxa, 361 at last count. This experiment can be repeated by anyone wishing to go to the trouble of doing it.

The rest of this post is standard, straight from the textbook. No heresy involved.

Evolution does its own thing
It’s fairly common knowledge that basal reptile genders are pretty similar internally. In other words, it’s generally hard to tell males from females. Often, the only difference is the substitution of uteri and ovaries for testicles. Externally a single opening, the cloaca (or sewer), expels urine, feces and eggs. The same holds true for basal mammals, like the egg-laying monotremes (Fig. 1, image from Peters 1991). The uterus is the organ that nourishes eggs and produces a secretion that hardens to form a shell around each one. In males an extensible penis was present for internal sperm deposit. It was not a conduit for urine at this stage.

Figure 1. Monotreme sex organs. There is very little difference here, other than the uteri and ovaries in place of internal testicles.

Figure 1. Monotreme sex organs from Peters 1991. There is very little difference here, other than the uteri (uteruses) and ovaries in place of internal testicles. That all changes in marsupials and placentals.

Marsupials (metatherians)
In marsupial females things are a little different. The rectum splits off from the urine and birth canal creating its own opening in the body wall. The birth canal is shorter than the cloaca and splits to form twin vaginas.

In most mammals (whales and manatees are notable exceptions) the testicles need to be kept cooler than body temperature, so in marsupial males the testicles are outside the body wall in a sac-like scrotum. The scrotum of the male and the pouch of the marsupial female arise from the same structure. Hormones turn them into distinct body parts during maturation.

In marsupials the penis becomes a urine channel as well as a sperm channel. The penis is generally kept within the body, extending only for mating. Here (Fig. 2) it is extended, and yes, it has two tips.

Figure 2. Placental mammal sex organs.

Figure 2. Marsupial and placental mammal sex organs.

Placentals (eutherians)
In placental females the twin vaginas fuse to become one. The uteruses (uteri) remain paired and their walls thicken to support larger embryos (fetuses). Humans have but one uterus, formed by the fusion of the pair.

Most male placentals “drop” the testicles slightly behind the penis from their origin near the navel in marsupials. The penis is typically outside the body wall, but often sheathed against the belly/abdomen. In bats and primates it become pendulous, losing its body wall attachment.

Most male placentals (eutherians) develop a bone (baculum, os penis) in the penis, which lends support during mating. This bone is still present in primates, but greatly reduced in the gorilla and chimpanzee, and, of course, lost in humans.

In other reptiles
The penis developed independently several otherwise unrelated lineages. Some turtles have them. Some birds have them. Others don’t. Crocs have a penis. Lizards and snakes have paired hemipenes. Sphenodontids do not have a penis. So, the situation in pterosaurs is a toss-up. Click here for a broadcast video (with lots of commercials) on dinosaur sex featuring some of your favorite paleontologists.

Peters D. 1991. From the Beginning – The Story of Human Evolution. Little Brown.