Evo-devo of digital reduction in amphibians

Synopsis: Alberch and Gale: “A Developmental Analysis of an Evolutionary Trend: Digital Reduction in Amphibians” (1985). In this paper, the authors looked at different foot morphologies in extant amphibians and performed some experimental embryology with a few of the species. The induced developmental change followed the natural variation found by the authors! Details below!

This post serves two purposes as:

1) My weekly devo post

2) Personal interest in the larger picture of evo-devo and how it relates to the Modern Synthesis. (Little surprise that I discovered this article through a Stoltzfus article!)

Alberch and Gale first examined the digital morphology, particularly the number of phalanges in hindlimbs, of extant amphibians. They excluded caecilians due to their limbless nature and focused on anurans (frogs) and caudates (salamanders). Interestingly, as of 1985, there was debate if frogs and salamanders are mono- or polyphyletic (meaning did the two groups arise from different ancestors)? This is due to different developmental pathways, one which we will explore here (although that is not the ultimate point).

Alberch and Gale focused on digital reduction and they noticed patterns within each taxa. This makes sense as frog digit development starts from the middle and proceeds outward while Salamander digit development is sequential – from I (“thumb”) to V (“pinky”). The pattern Alberch and Gale noticed was that frogs initially lose I and V (the outer digits), whereas salamanders lose V/IV (the last digits). This is shown in frogs in Fig 1.

The authors further decided to mess around with the developmental process by adding colchicine, a mitotic inhibitor, to the developing limb bud, subsequently reducing the number of cells found within. The patterns of the “mutated” (these aren’t genetic changes) limb buds followed the natural morphological patterns!

Fig 2: a) Dorsal view of the left foot of salamander Hemidactylium scutatum (a 4-toed lungless salamander). b-c) The two feet of a fully developed axolotl Ambystoma mexicanum. The right foot (c) is the untreated control, while the left foot (b) has been treated with colchicine at the limb bud stage. Notice the left foot (b) is smaller than the right foot (c), and also notice that the morphology of (b) closely resembles (a), a foot of a different species, in digit number and phalanges number per digit. Also note the differences in the tarsals.

Figure 2 is particularly evocative. By messing with the left limb bud of (b) (same species as c)), the resulting foot resembles that of a), a different species. Specifically, the phalanges number per digit is the same between a) and b):

The phalanges formula (from I to V) (take heed of the mirror images of Fig 2):

a) 1-2-3-2-0
b) 1-2-3-2-0
c) 2-2-3-4-2

That is a major difference. Also notice that b) is physically smaller than c), which is not surprising considering colchicine reduces the number of cells available to the developing limb bud.

Is this a case of “simple developmental truncations”? In other words, are these differences a result of development just stopping at a certain point? This is possible considering the salamander is losing digit V (remember sequential development), but Alberch and Gale argue no. Here is why.

Fig. 3: Sequence of metatarsal and phalangeal differentiation in the salamander, A. mexicanum (the changed species from Fig. 2). Stippling indicates early stages of chondrogenesis (cartilage formation).

Look at normal left foot development (Fig 3) in Ambystoma mexicanum (the axolotl changed in Fig 2). If development were to stop before the formation of digit V (the leftmost digit in this figure), the foot would be somewhere between the 4th and 5th depicted stages. The resulting phalanges formula would be 2-2-3-1-0. However, as we saw in Fig. 2, the resulting foot due to the “mutation” is 1-2-3-2-0. Clearly the two do not match. This is depicted in a different species in Figure 4c and 4d. (Fig. 4a and 4b depict the change of Fig. 2).

So “simple development truncation” does not support the results. Instead, Alberch and Gale state that mutations would have to affect the limb bud in similar ways to the mitotic inhibitor, colchicine. Examples include dwarfism (reduce the absolute number of cells) or a “slowdown in the rate of cell proliferation associated with paedomorphosis. Dwarfism may be likely as evidenced by Fig. 2 and by more data collected by Alberch and Gale.

Alberch and Gale (and subsequently, Stoltzfus) argue for a larger idea which I will discuss in my next weekly devo post (this one is long already!). Alberch and Gale argue we must revise how we think of developmental constraints. In turn, Stoltzfus argues that the Modern Synthesis cannot take these developmental biases into account and that we must come up with a new synthetic theory of evolution. Find out why next week!
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Alberch, P., & Gale, E. (1985). A Developmental Analysis of an Evolutionary Trend: Digital Reduction in Amphibians Evolution, 39 (1) DOI: 10.2307/2408513