Exercise 10.1

Sexual Selection, Developmental Thresholds, and Ornamentation

(This exercise is based on Rowland, J. M., and D. J. Emlen. 2009. Two thresholds, three male forms result in facultative male trimorphism in beetles. Science 323: 773–776.)

(Note: The reference above links directly to the article on the journal’s website. In order to access the full text of the article, you may need to be on your institution’s network [or logged in remotely], so that you can use your institution’s access privileges.)

INTRODUCTION

In Chapter 10 you read about how sexual selection can drive the evolution of bizarre and sometimes costly ornamentation or weaponry in animals, often in males. This paper reveals a situation where sexual selection is the driver, but the result is more complex than might be expected at first glance. The authors describe some beetle species where different thresholds encountered as larvae result in different levels of ornamentation, and consequently different reproductive strategies.

The authors show that in one family of beetles (the Scarabeidae [dung beetles]), two different threshold mechanisms have independently evolved. Each of these thresholds has a different effect on horn development in the males of these beetles. Both mechanisms are triggered by body size in larvae. For one mechanism, if a larva attains the threshold size its adult morphology (the phenotype it will have after it pupates) switches from being hornless to being horned. The second threshold, also based on larval body size, similarly results in either having a short or a long horn (see Figure 2).

This discovery led the authors to look more closely at other beetle species where male polymorphism was known to occur, and they found two other examples where this double threshold mechanism was operating (see Figure 1). In the family Lucanidae (stag beetles), they found that male trimorphism was characterized by differences in the mandibles, with male mandibles exhibiting three increasing sizes moderated by the thresholds. In the family Curculionidae (weevils), the thresholds controlled the development of ventral body spines. Here, the beetles either lacked spines (and thus resembled females), had short spines, or had long spines.

The authors suggest that this multiple-threshold system may be more prevalent than previously thought, and anticipate more examples coming to light.

QUESTIONS

Question 1. What are polyphenic regulatory developmental mechanisms?

Question 2. Can you think of an example of polyphenic regulatory developmental mechanisms besides the beetles mentioned in this paper.

Question 3. The authors use the “rock-paper-scissors” analogy to describe the potential result of this two threshold system when it comes to reproductive success in dung beetles. As in the game of rock-paper-scissors, each possible pair-wise comparison has a clearly defined winner. Give a hypothetical example of what this might look like in the context of dung beetle mating success.

Question 4. What is the difference between the systems described in this paper and the other examples of male trimorphism cited by the authors (in isopods, lizards, and birds)?

Question 5. Why might a trimorphic system such as this evolve? Why wouldn’t natural selection just drive all males to have the biggest possible horn, spine, or whatever the ornament involved is?

Figure 1 Male trimorphism in three beetle families. (A) In scarabaeid dung beetles (Oxysternon conspicillatum), alpha and beta males both produce head horns, but the relative sizes of these weapons differ (shift in intercept of the scaling relationship between horn length and body size, threshold mechanism 2). Gamma males and females lack head horns entirely (change in scaling relationship slope, threshold mechanism 1). Alpha, beta, and gamma males were discriminated by the likelihood method for normal distributions (25). (B) In lucanid beetles (Odontolabis cuvera), male mandibles occur in three discrete anatomical conformations, which identify the alpha, beta, and gamma male forms (also fig. S2). (C) In weevils [Parisoschoenus expositus; measures from (26)], males produce long ventral spines that are outgrowths of the sternum and flank a deep invagination of cuticle, the sheath. As with the dung beetles, alpha and beta males produce similar weapons that differ in relative size (threshold mechanism 2), whereas gamma males lack weapons and resemble females. In P. expositus, gamma males and females lack both the ventral spines and the sheath (white arrows) used in male combat (26).

Question 6. Looking at Figure 1B, does mandible length in alpha males vary with body size at approximately the same rate (slope) as it does with gamma males?

Question 7. Looking at Figure 1A, does horn length in alpha males vary with body size at approximately the same rate (slope) as it does with gamma males?

Figure 2 Two threshold mechanisms regulate expression of horns in male dung beetles. (A) Horn length/body size scaling relationships for natural populations of adult males of Phanaeus igneus (left), P. triangularis (middle), and P. vindex (right) reveal these processes as an abrupt and size dependent change in scaling relationship slope (threshold mechanism 1, left), a size-dependent shift in intercept (threshold mechanism 2, right), or a combination of the two mechanisms (middle). Because among-individual variation in body size in scarab beetles is influenced primarily by larval nutrition, species simultaneously incorporating both of these threshold mechanisms are facultatively trimorphic. From this, we define alpha (light blue), beta (dark blue), and gamma (green) male forms, which were discriminated by the likelihood method for normal distributions (25). (B) Evolution of two thresholds mapped onto a phylogeny of 22 species of phanaeine scarabs [tree topology from (34)], with the presence of each threshold mechanism (bold branches) estimated by parsimony (35). Species containing alpha, beta, and gamma male forms indicated as above. Facultative trimorphism appears to have been gained at least four separate times in the period covered by this phylogeny (red boxes).

Question 8. In the phylogeny shown in Figure 2, how many species lack males that grow horns?