Last week, I received some delusional e-mail from Phil Skell, who claims that modern biology has no use for evolutionary theory.

This will raise hysterical screeches from its true-believers. But, instead they should take a deep breath and tell us how the theory is relevant to the modern biology. For examples let them tell the relevance of the theory to learning…the discovery and function of hormones…[long list of scientific disciplines truncated]

Dr Skell is a sad case. He apparently repeats his mantra that biology has no need of evolution everywhere he goes, and has never bothered to actually crack a biology journal open to see if biologists actually do use the theory. In my reply to him, I did briefly list how evolution is used in every single one of his numerous examples, but today I’m going to focus on just the one I quoted above: hormones.

Now I’m not an endocrinologist, and I don’t usually read much in the hormone literature, so it was just chance that I stumbled across a review article on this very topic in BioEssays. My point is that you don’t have to be an expert in the discipline to find evidence that Skell is completely wrong; all it takes is a casual perusal of the general scientific literature and a prepared mind (alas, I fear that creationists don’t do the first and lack the second. One of the reasons I am concerned about science education in grade schools is that one of the aims of the creationist movement is to make sure our kids lack prepared minds, too.)

The review paper by Heyland et al. (2004a) is well worth looking up. It has a long introduction that covers several important themes in modern evo-devo, that I’ll just summarize briefly here.

• Modularity. This is a complicated idea with many permutations and some peril of over-extension (see West-Eberhard (2003) for a thorough discussion.) What we see over and over in development, though, is discrete, dissociable subsets of gene regulatory networks that are re-used and modified to fulfill various functions. They are molecular building blocks that organisms use in diverse ways to build embryos.
  Modularity complicates homology in interesting ways, though. In the case of hormone evolution, it means that many species have a module of homologous proteins that manage signalling for a particular hormone, but how that module is plugged into the rest of the cellular circuitry varies—in some species it may activate another function, and in others it may repress it.
• Cooption. Add this one to your list of synonyms. First there was the term “preadaptation” with its unfortunate teleological implications; then Gould & Vrba coined the better term “exaptation”; nowadays the magic word you hear most used by developmental biologists is “cooption.” The idea here is that modules get coopted, or used in novel circumstances, to generate new functional and morpholical properties.
• Life History Transitions (LHTs) and Life History Evolution (LHE). One of the hot topics in evo-devo is a conceptual move, to stop regarding adult forms as the target of evolution and instead regard species more holistically, as the sum of all of their stages of development. A tick, for instance, is more than just the nasty parasite that sucks your blood; it may also have distinct and amazingly complex life cycles in which it lives in different environments and has radically different feeding strategies, and we have to take all of them into account in understanding their evolution. Arthur’s Biased Embryos and Evolution is an excellent primer on the importance of life history evolution.
• Model Systems. As a guy who works with a model system, the zebrafish, the evo-devo argument against them always makes me a little uncomfortable, because they are largely right. Model systems are great for plumbing deeply into the details of an organism, but the flaws are that model systems are rarely very representative (Danio is a weird little specialized fish, no doubt about it), and that you must at some point explore comparative aspects of their development if you want to discuss evolution.

Heyland et al. tie all this together to help us understand what is going on in the evolution of hormone signaling systems. Their general point is that hormones are key regulators of life history transitions across the animal and plant kingdoms, that we need to survey an array of lineages rather than single model systems to get an appropriate perspective, and that when we do, we see examples of cooption all over the place. The review mentions many examples, but their own work is concentrated on echinoderm evolution.

Some of these ideas are shown in the table below, which lists metazoan phyla and shows which classes of hormones they use to regulate life history transitions. These things are ubiquitous, and as a broad principle it’s clear that hormone signalling pathways have been coopted throughout evolutionary history for this function.

(click for larger image)
Wide-spread involvement of hormones in life history transitions (LHTs). “+”indicates that this class of hormones has been demonstrated to be involved in a LHT [hatching, larval transitions, resting stages (such as dauer and diapause), metamorphosis, settlement, migration, attainment of reproductive maturity and ovulation/oviposition]. “?” indicates that such a role has not been demonstrated for that phylum. “+? indicates preliminary evidence for such a role. Note that the four large hormone families considered here do not encompass all animal hormones involved in LHTs; certain hormones were omitted for simplicity. Also, hormones belonging to the same family can be synthesized by vastly different biochemical pathways. Furthermore, the original sources of animal hormones might have been plants/algae in many cases, and could well have been independently derived from plants/algae in distinct lineages. Finally, different taxa use similar hormones to regulate totally different LHTs (such as steroids in molluscan reproduction and arthropod molting) and, in some cases, the same hormone has been coopted multiple times to regulate independently evolved metamorphoses (TH is the prime example). For these reasons, the reader should not interpret the presence of a similar class of hormones in related animal taxa to be sufficient evidence for common ancestry of particular LHT functions and their hormonal control. (numbers in table refer to references).

One might argue that maybe the hormone function evolved once, that the ur-metazoan had a life history transition regulated by, for instance, thyroid hormone, and that therefore all metazoan metamorphoses are actually homologous. This is not supported by the data—metamorphosis has evolved multiple times, and each time a common signaling pathway has been recruited to help do the job. For instance, frogs require increased thyroid hormone levels as a trigger for metamorphosis; lampreys, on the other hand, require a period of reduced TH levels for their transition. That the pathways work in different ways in these two lineages is evidence for independent acquisition of the role for TH.

Another feature the authors explored were the radical differences in metamorphosis in some echinoderm lineages. The stereotypical pattern of development in the echinoderms is that the embryo first develops into a feeding pluteus larva, a tiny ciliated beast that swims about consuming food and growing, before making a transition to the more familiar sea urchin or starfish or sand dollar form. This is called indirect development. Some species, however, skip the feeding larva stage completely, and the embryo settles down on the sea floor and develops directly into the adult form; this is called, obviously enough, direct development. As you can see in the diagram below, different lineages may exhibit all indirect development (“all feeding”, the green boxes), all direct development (“all non-feeding”, the one gray box for echinothuroid urchins), or most complicated of all, a mixture of direct and indirect development in different species (the yellow boxes).

Life history strategies in echinoids (Echinodermata). It is generally accepted that a feeding mode of development is ancestral for the echinoids, but non-feeding development has certainly evolved many times independently in the group. These multiple independent evolutionary transitions provide fertile ground for studying the mechanisms underlying LHTs and LHE.

Obviously, a sensible cladogram can’t be built from the direct vs. indirect development character—this is a developmentally labile feature. The best known example of this surprising difference is from the work of Raff’s lab, which has been studying two sister sea urchin species in the genus Heliocidaris. H. erythrogramma is a direct developer, going straight from embryo to adult form, while the closely related H. tuberculata is an indirect developer with a feeding pluteus larva.

This is a radical morphological change that greatly changes the pattern of early development. What Heyland et al. demonstrate, though, is that it may require nothing more than a shift in the timing of a hormone. The trigger for echinoderm metamorphosis is the usual suspect, thyroid hormone. They found that they could transform individuals of a sand dollar species, Leodia sexiesperforata, which has an obligate larval feeding stage (that is, the animals die if they can’t eat as larvae) into facultative feeding larvae (they can survive and undergo metamorphosis without a meal) by simply treating them with TH. One simple exaptation that can lead to a shift from indirect to direct development is an upregulation of TH production.

The lesson the authors are trying to leave us with is that hormone signaling is a rich field to study within an evolutionary context, and that the pattern of hormone use tells us a great deal about origins and mechanisms of evolutionary novelties.

Hormones coordinate life history transitions in a wide variety of animal and non-animal taxa, and similar hormones have been repeatedly coopted in independently evolved life history transitions in disparate taxa (an example of homoplasy). Derived life histories, such as vivipary in plants and the evolutionary loss of larval feeding in echinoderm larvae involve alterations in these same hormones. We suggest that it is the modular nature of hormonal signaling systems that predisposes them to be used in these diverse developmental and evolutionary contexts, and propose a broadly comparative, non-model system approach to illuminate evolutionary patterns in organismal ontogenies.

This is the kind of thing that leaves me scratching my head when a creationist announces that “the discovery and function of hormones” is not a subject that is enlightened by evolutionary theory. It really isn’t at all difficult to find work that integrates evolution and endocrinology, and for which evolutionary explanations are indispensable.

Arthur W (2004) Biased Embryos and Evolution. Cambridge University Press.

Heyland A, Hodin J, Reitzel AM (2004a) Hormone signaling in evolution and development: a non-model system approach. Bioessays 27:64-75.

Heyland A, Reitzel AM, Hodin J (2004b) Thyroid hormones determine developmental mode in sand dollars (Echinodermata: Echinoidea). Evolution & Development 6(6):382-392.

Nielsen MG, Wilson KA, Raff EC, Raff RA (2004) Novel gene expression patterns in hybrid embryos between species with different modes of development. Evol Dev 2(3):133-144.

West-Eberhard MJ (2003) Developmental Plasticity and Evolution. Oxford University Press.