Just as the examples supporting evolution in general have grown tremendously in both number and variety since Darwin’s time, so have the cases supporting trait loss. Here, we cover five well-studied cases of trait loss that either illustrate an important principle or would be likely to catch the attention of students.
The Silence of the Crickets
On a quiet night, walk outside. If the temperature is high enough, you will likely hear crickets chirping. Males of most cricket species produce these chirps in order to attract and secure mates. Sound production arises when a male rubs its forewings together in a process known as stridulation. Curiously, in a Hawaiian population of the Polynesian field cricket, Teleogryllus oceanicus, such sounds have been greatly diminished. Why have the crickets gone silent?
Native to Australia, the Polynesian field cricket migrated eastward to oceanic islands, reaching Hawaii sometime before 1877. In Hawaii, a parasitoid fly, Ormia ochracea, is attracted to the male song. Thus, males who sing run a much greater risk of parasitism. Parasitism from the fly, which is not found in the native range of the cricket, has altered the singing behavior of males where the fly is present. In an extreme case, a morphological mutation causes males to lack the structures on the forewing that are needed for song; thus, males with this mutation are silent. This mutation, called flatwing is likely adaptive. On the Hawaiian island of Kauai, the frequency of flatwing increased from near zero to 91% between the late 1990s and 2004 (16–20 generations) (Zuk et al. 2006).
Results from a preliminary genetic analysis (Tinghitella 2008) are consistent with flatwing being a mutation at a single X-linked gene. The genetic basis of this trait is of interest as a sex-linked allele that is expressed in the heterogametic sex (the one with two different types of sex chromosomes) would be conducive to a rapid increase in frequency, as opposed to a trait that had a polygenic basis.
Given that the flatwing males don’t sing, how do they find and attract mates? The flatwing males act as satellite males: they wait for other males to sing, approach those males, and then attempt to mate with females attracted to the singing male (Zuk et al. 2006; Tinghitella and Zuk 2009). Mating preference tests by Tinghitella and Zuk (2009) revealed that females are significantly less likely to mount flatwing males. This preference varies across populations; however, females from populations with flatwing reject flatwing males less than do females from populations without flatwing males. There is no significant heterogeneity for female preference among the different populations that have male song. Tinghitella et al. (2009) showed that male satellite behavior preceded the origin of the flatwing mutation and evolved independently of it.
Singing males face a very high risk of parasitism, but the satellite males that take advantage of the singing males do not face this risk. Obviously, this strategy cannot persist if there are no singing males, so the advantage of the flatwing males who are forced to be satellites will be lost if the percentage of singing males drops too low. This situation sets up the prospect for frequency-dependent selection maintaining an equilibrium, wherein both types of males are maintained at more or less constant frequencies. The exact frequencies of the two types of males will depend on the magnitude of the parasitism pressure and the nature of the mating disadvantage to satellite males when singing males are rare.
In the Polynesian field crickets of Hawaii, the changed environment due to the presence of the parasitoid led to natural selection directly favoring the loss of song, a trait under sexual selection. This loss occurred by a morphological mutation affecting wing structure instead of a behavioral suppression of the song. Loss of traits that originally evolved due to sexual selection is a common phenomenon (Wiens 2001). For instance, phylogenetic analysis of 47 genera of fruit-eating birds known as tanagers reveals that evolutionary changes from colorful males to drab males are about five times more frequent than changes from drab to colorful. In at least some of these cases, the loss of the sexually selected trait correlated with changes in environmental conditions. A common environmental change resulting in the loss of sexual displays is a new parasite or predator that would be attracted to the display, as the parasitoid wasp is to the song of the Polynesian field cricket. Another circumstance in which a sexually selected trait might be lost is if the transmission of the signal is hindered. For example, some African rift lakes have become polluted such that their waters are murky. If the visibility is so poor that female cichlid fish can no longer see the male color displays, this will reduce or relax selection maintaining the bright male colors and they may fade, even leading to mating confusion among species (Seehausen et al. 1997).
Better Living Without Sex?
From an evolutionary perspective, the mating systems of plants are rather changeable, as plants that engage in sexual reproduction often have close relatives that are asexual. Moreover, even within species, some populations may be fully sexual while others are completely or mostly asexual (Eckert 2002). The causes of such variation include both physical and biotic features of the environment, which are often unknown. Interestingly, in species that vary with respect to sexuality, asexual reproduction is often found at the periphery of the species range (Eckert 2002). At the edge, population sizes are usually lower and the match between the plant’s adaptations and the environments are usually less good than in the main portion of the species’ range (e.g. Eckert et al. 2008).
Swamp loosestrife Decodon verticillatus is one example of variation in mating systems. This perennial, aquatic plant is found in wetlands in eastern North America. Sexual reproduction occurs in this species via insect-pollinated flowers, and asexual reproduction occurs via adventitious rooting of branch tips. Throughout most of its range, most populations of D. verticillatus reproduce sexually. Across the northern part of the range of this species, from northwestern Massachusetts through southern New Hampshire and up along the Maine coast, most populations are asexual, and the loss of the capacity to reproduce sexually (sexual sterility) appears to have arisen several times. The asexual populations have much lower genetic and morphological variability than the sexual ones, though it is not clear whether the loss of sex led to the lower genetic variability or vice versa (Dorken and Eckert 2001).
What evolutionary hypotheses account for the loss of sex in these northern populations of D. verticillatus? We can distinguish three general hypotheses: mutations that cause the loss of sex are (1) neutral and neither increase nor decrease fitness, (2) advantageous because they enhance asexual reproduction either by freeing up resources or by some other means, or (3) are deleterious but become fixed due to what is known as the mutational meltdown (Eckert 2002). In the mutational meltdown, deleterious mutations accumulate because the population size is low and thus subject to strong genetic drift (Lynch 2007). Populations at the periphery of species ranges would be most likely to encounter a mutational meltdown scenario because they are more subject to population bottlenecks and the associated strong genetic drift. The lower variability of the asexual populations (Dorken and Eckert 2001) is consistent with, but not proof of, the mutational meltdown.
One way to test these competing hypotheses would be to compare how well the sexual and asexual populations do in asexual “vegetative” growth and reproduction in the same setting (a “common garden experiment”). If the loss of sex is due to mutational meltdown, vegetative growth should be lower in the asexual population. The neutral mutation hypothesis would predict that the populations would have equivalent vegetative growth rates, and the advantageous mutation hypothesis would predict that the asexual populations would actually have higher vegetative growth. With such a common garden experiment, Dorken and colleagues (2004) showed that sterile genotypes have a fitness advantage in asexual populations, thus supporting the hypothesis that the loss of sex is actually advantageous at least under some circumstances. Exactly what this advantage is, and the ecological circumstances that led to this plant losing the ability to reproduce sexually, are subjects for future inquiry.
No Eyes Are Better than Two
An estimated 100,000 species of animals live in caves. Since before Darwin’s time, biologists and naturalists have been fascinated with the unusual convergent adaptations to life in caves as well as the loss of previously adaptive traits, such as eyes and skin pigments that no longer provide an advantage in the absence of light (Culver et al. 1995). The adaptation to darkness, including the loss of these traits, is called troglomorphy.
The Mexican “blind cavefish” (a form of the tetra Astyanax mexicanus) is emerging as a model system for the study of cave organisms and the evolution of troglomorphy (reviewed in Espinasa and Espinasa 2008; Jeffrey 2009). Unlike most cave-dwelling animals, A. mexicanus is fully fertile with surface populations and can be bred in the lab; thus, the features of this species associated with cave life are easily amenable to genetic analysis. Moreover, this species can be found in about 30 caves in Mexico, raising the prospects for multiple incidents of independent evolution. Molecular phylogenetic studies (Jeffrey 2009) indicate that the caves were settled at least three (and possibly four) independent times and that eyes were lost independently several more times, demonstrating parallel and convergent evolution.
Simple genetic analysis can reveal information about the nature of the evolution of eye reduction. For instance, eyes in the hybrids in F1 crosses between some different cave populations are substantially larger than those of the parents (Wilkens and Strecker 2003). This finding is evidence that some of the genetic changes that have led to eye reduction differ across the cave populations and act in a mostly recessive manner. Why would that be the case? Consider the simple situation wherein the two populations evolved reduced eye size and that the reduction was due to different recessive alleles (a and b) at different genetic loci (A and B, respectively). The two populations would have genotypes aaBB and AAbb. Hybrids between the populations would be AaBb, and thus would have wild-type-sized eyes. Even in more complex situations where more than two loci are involved and the dominance relationships are not complete, hybrids would still have larger eyes than the parental populations if different genetic changes were responsible for the eye reduction in the two populations and the eye-reducing mutations are mostly recessive. In contrast, if the same genetic changes had occurred in the different populations or had the eye-reducing alleles been dominant, then the F1 hybrids between cave populations would have eyes roughly the same size of those of their parents.
More sophisticated studies of the genetic architecture of eye size differences rely on quantitative trait locus (QTL) analysis. In this commonly-used technique, a series of crosses between two extreme forms (in this case, the surface populations and the cave populations) generate a sample of organisms that vary both in genotype and in the trait of interest (see Conner and Hartl 2005 for a review). Some of the genes of these individuals derive from the surface population, the rest of their genome derives from the cave population, and different individuals vary in the sources of their genetic material. A series of genetic markers, usually DNA-based, then determine whether a particular individual has cave or surface genetic material at a given location in the genome. If individuals that have surface population DNA at a given location in the genome tend to have larger eyes than individuals that have cave population DNA there, then this region is likely a gene or is near a gene that influences the eye size difference between the two forms. Such QTL analysis has revealed several regions of the genome that influence eye size differences between cave and surface forms (Jeffrey 2009; Protas et al. 2008). Among these is a region near the sonic hedgehog (shh) gene.
What evolutionary forces have led to the degeneration and loss of eyes in this cavefish? Darwin (1859) speculated about the evolutionary reasons for eye loss and degeneration in caves. He noted, “As it is difficult to imagine that eyes, though useless, could be in any way injurious to animals living in darkness, I attribute their loss solely to disuse.” At least for A. mexicanus, Darwin’s explanation appears incorrect. Similar to the case for loss of sex in Decodon verticillatus (see above), loss of eyes appears to be advantageous: evidence suggests that eyes are costly because their development reduces the resources available for at least one other sensory system (Jeffery 2009). Specifically, eye precursors and taste receptors share some developmental underpinnings such that scaling back the eyes allows for greater development of taste receptors (Yamamoto et al. 2009). Cave and surface A. mexicanus differ in the expression levels of several genes, including the gene sonic hedgehog (shh) whose expression is higher and differently situated in cavefish than in surface fish. Interestingly, shh is involved in the eye/taste bud differentiation: overexpression of shh decreases eye formation but increases taste receptors and other aspects of the olfaction system and the jaw. Inhibition of shh leads to the opposite: decreased development of taste buds and jaws, but increased eye formation. Moreover, QTL analysis shows that the QTLs found in crosses between surface and cave populations are all in the same direction (the surface allele increases eye size and the cave allele decreases it) (Jeffrey 2009; Protas et al. 2008). This pattern is strong support for the action of natural selection operating on the trait (Orr 1998). These clues point to a possible evolutionary mechanism: natural selection operated to increase taste receptors and jaw size through changing the expression of shh (and likely other genes). The increased shh expression had the pleiotropic consequence of leading to decreased eye development. Indirect selection is the term that refers to this phenomenon of a change in one trait occurring through selection on a correlated trait. Indirect selection may play a role in the loss of many traits in nature (Lahti et al. 2009).
In the extreme dark, vision has little utility; thus, eyes would not be of much selective value. In both dark and the light environments, the ability to taste and strong jaws are beneficial. In the light, there is a tradeoff between the developmental precursors of eyes on the one hand, and taste buds and jaws on the other; thus, the optimum in light environments is to compromise and funnel resources to both. In the dark, however, resources spent on eyes are wasted; thus, genetic changes that lead to fewer resources devoted to eyes are selectively advantageous.
When Legs Get in the Way
Whales and snakes provide among the most fascinating and recognizable cases of trait loss. The fact that these legless animals (among others) descended from typical tetrapods with four limbs provides an excellent angle for evolutionary education. Unlike the previous three situations, whose examples and evidence are primarily extant organisms and can be studied by field evolutionary ecology and laboratory experimentation, limb loss in vertebrates occurred many millions of years ago, and phylogenetic and paleontological studies have played a much larger part in our understanding of these events. Here, we briefly highlight the evolution of hindlimbs and locomotion in the whale lineage.
The cetaceans, an order comprised of the whales, dolphins, and porpoises, descended from land-walking four-limbed ancestors about 50 Mya (million years ago) (Xiong et al. 2009). Only recently have many of the details of their evolution come to light (see Fig. 2), through fruitful deposits of fossil material, such as several sites in Pakistan (Gingerich et al. 2001, 2009). Overall, the picture is one of an increasingly aquatic existence over a period of about 12–15 Mya, accompanied by “mosaic evolution” of several different kinds of traits. While some traits such as echolocation, blubber, and the tail fluke newly evolved, other traits such as hindlimbs and fur were reduced or lost. Limb loss in whales was probably fostered by natural selection for swimming efficiency, because a vertical undulation (the locomotive strategy of cetaceans) is optimized with a hydrodynamic form, and legs would only get in the way (Thewissen 1998). Other traits remained but changed form: nostrils shifted backwards and upwards, and forelimbs turned into flippers. And, of course, body size greatly increased. All of these changes related to or were facilitated by life in the water (Bejder and Hall 2002). This scenario illustrates the important fact that trait loss does not represent or require a fundamentally different kind of evolution than we see in traits that are growing or changing in other ways. We advocate an increased focus on trait loss not because it involves unprecedented mechanisms, but because it is often overlooked in evolutionary education whereas, as the whale situation shows, it is just as much a part of major evolutionary transitions as other sorts of trait changes are.
The developmental mechanisms that underlie trait loss provide potent case studies of the way in which evolution and development interact. In only the most extreme cases does an entire developmental sequence relating to a trait disappear, as in the loss of teeth in cypriniform fish, for instance (Stock et al. 2006). In perhaps most cases, early development of the trait proceeds but is eventually halted. In embryos of modern cetaceans, limbs do begin to develop, but they later disintegrate. For instance, developmental evidence from dolphins demonstrates that limb buds develop normally in the first few weeks, but then shrink in later embryonic development (Sedmera et al. 1997; see Fig. 3). Comparative embryology was one of the earliest sources of evidence for evolution, and still today results like this can be used to solidify students’ understanding of evolution, and in particular the “tinkering” nature of evolution—the fact that current traits do not start from scratch but from precursors. The case of whale limb buds can now be added to other well-known cases, such as our pharyngeal gill arches, where the traces of ancestral trait loss remain in the embryos of modern organisms.
The Mysterious Appendix
When people think of a vestigial trait, the human appendix often comes to mind. Indeed, the word appendix also refers to parts of a book or article that are set apart from the main text, and could be skipped without major loss of understanding of the work. Ironically, the mammalian appendix may not be vestigial organ, but actually serve a function.
The appendix has been viewed as an expendable organ because it can be removed (appendectomy) without causing any apparent loss of function. Appendectomies are performed because appendices can become inflamed (a condition known as appendicitis). If left untreated, this inflammation can lead to death. Although it can occur at any age, appendicitis is most common in older children, teenagers, and young adults. A 1990 epidemiological study estimated the lifetime risk of acquiring appendicitis at 8.6% for males and 6.7% for females in the United States (Addiss et al. 1990). As we will discuss below, the incidence of appendicitis has dropped since 1990, but a sizeable fraction of people still develop inflamed appendices. Interestingly, the lifetime risk for having an appendectomy is much higher than the risk of appendicitis, especially in females (Addiss et al. 1990).
Appendicitis increased in frequency during the nineteenth and early twentieth centuries, peaking during the late 1920s (Kang et al. 2003). Starting around 1930, its incidence has declined in the United States, the UK, and other industrial countries. This downward trend has continued at least through the 1990s, and is not explained by changes in medical practices, such as diagnoses (Kang et al. 2003). Among the first to note the decline in appendicitis was Kenneth Castleton, who was struck by the dramatic decline in the death rate from appendicitis in post-war America. He noted that the annual appendicitis-related death rate had fallen from 8.1 per 100,000 in 1941 to 1.3 per 100,000 in 1956 (Castleton et al. 1959). Castleton questioned whether the six-fold decrease could be explained solely by the use of antibiotics and other improvements in medical care or if the actual incidence of acute appendicitis. Surveying a wide range of hospitals, Castleton and colleagues found that the actual incidence had fallen by roughly two-fold, both in urban and in rural hospitals.
Castleton, like many before and after him, was at a loss to explain such a decline, and suggested nutritional factors and the use of antibiotics might be behind it. Of course, as Kang et al. (2003) point out, the decline in appendicitis incidence had begun before antibiotics were used by a large segment of the population. Kang et al. (2003) also present some of the historical reasons given for both the rise and fall of appendicitis rates. In summary, physicians have frequently tied appendicitis to diet, though often without much supporting evidence. Some evidence does support that tomatoes and some leafy vegetables may protect against inflammation of the appendix, but the data supporting this conclusion are correlational (people who eat those vegetables and tomatoes have lower rates of appendicitis), but not causal (Kang et al. 2003). Even now, we don’t have a good understanding of either why appendicitis rose in frequency in the nineteenth century or why it fell through most of the twentieth.
So why do we have appendices in the first place? One intriguing hypothesis presented by Bollinger et al. (2007) is that the appendix evolved as a storehouse for biofilms of commensal bacteria. Following Scott (1980), they argue that appendix-like structures are relatively rare and scattered throughout the phylogeny of mammals, present in rabbits, opossums, and wombats in addition to humans and closely related primates. Such a pattern is suggestive of a structure that evolved for a specific function. Bollinger et al. also argue that the structure of the human appendix is well suited for the formation of biofilms of bacteria, as well as protection of said biofilms.
So, why does the appendix present problems for a relatively small, but not insignificant minority of people? A likely explanation is that the appendicitis was not a major health problem for most of the evolutionary history of our species, but that changes in the environment (diet? changes in parasite load?) have made it so. Thus, according to that explanation as well as the dietary explanations given for its rise and subsequent fall in frequency, appendicitis is a condition of mismatch between the environments in which we evolved and those in which we dwell.
While intriguing and supported by some data, the biofilm hypothesis has not been fully confirmed. Moreover, other hypotheses also exist. One alternative is that the appendix does not serve a function, but that further reductions in its size would enhance the likelihood of appendicitis because smaller appendices were more likely to be infected (Nesse 1994). If this hypothesis were true, it would be an example of the limitations of evolution: no appendix would be ideal, but we can’t get there from here. Unfortunately, we currently lack the data to test this hypothesis.