Stalk-eyed Flies Research Articles

Sequential Analysis Reveals Behavioral Differences Underlying Female-Biased Predation Risk in Stalk-Eyed Flies

Stalk-eyed flies are classic models of how sexual selection can drive morphological and behavioral elaboration. Exaggerated ornaments born by stalk-eyed flies could impose locomotor costs and increase susceptibility to predation; however, a previous study determined that behavior, not eye span, was the major influence on predation risk. Despite the importance of behavior, relatively little is known about how these flies avoid and deter predators. We created an ethogram of behaviors and used it to score individual interactions of male and female Teleopsis dalmanni paired with an actively foraging, generalist arachnid predator (Phidippus audax). Sequential analysis was employed to identify temporal patterns in behavior and determine how males and females differ in their approaches to avoiding predation. Our results indicate that males and females significantly differ when specific behaviors were employed. Patterns in the behavioral transitions suggest that males are more aggressive than females and are more likely to approach a predator to jab, abdomen bob, or display. Males elicited more retreat responses from the predator, whereas females elicited more attacks. Although the behavioral repertoires of male and female stalk-eyed flies are indistinguishable, their uses of the behaviors differ, particularly the sequential order of presentation, suggesting a strong sex difference in anti-predatory behavior.

Rediscovery and Range Extension of the Stalk-eyed Fly, Sphyracephala subbifasciata Fitch (Diptera: Diopsidae) in Colorado and Wyoming

This paper reports on recent collections of the stalk-eyed fly, Sphyracephala subbifasciata Fitch in northeastern Colorado during 2010 and northwestern Wyoming during 1990. The Wyoming record extends the distribution of this family westward by almost 1200 km, and is the first confirmed record of the species in that state. For many years it was thought that only a single species of Diopsidae, S. brevicornis (Say, 1828), occurred in North America with S. subbifasciata as a synonym (Sabrosky, 1965; Peterson, 1987). However, Feijen (1989) recognized S. subbifasciata as a valid species. Fitch (1855) described S. subbifasciata originally from Illinois. Feijen (1989) subsequently recorded S. subbifasciata from southeastern Canada south to Maryland, west to South Dakota and Colorado. During an insect biodiversity survey of the Soapstone Prairie Natural Area (SPNA) in northeastern Larimer Co., Colorado a single female specimen of S. subbifasciata was collected on 3 October 2010 by the first author. Previously the only other Colorado specimens known were five specimens from Fort Collins, Colorado collected in 1895 (Feijen, 1989). This specimen of S. subbifasciata was collected by sweeping emergent stream and streamside vegetation, primarily Mentha species and grasses, along Spottlewood Creek in the SPNA, located 40 km north of Fort Collins. The Wyoming record of S. subbifasciata, a single male, was collected by the noted dipterist, Professor Robert Lavigne, while sweeping vegetation by Crayfish Creek, in Yellowstone National Park, Teton County, Wyoming. This specimen was collected on 14 June 1990. This specimen extends the known range of S. subbifasciata approximately 1200 km westward from Grand Forks, North Dakota and Kansas City, Kansas to Yellowstone National Park, Wyoming. We provide photographs (Fig. 1) of S. subbifasciata to facilitate identification and to encourage others to collect this interesting and uncommon fly in Rocky Mountain region. Currently, only ten specimens are known from this region including the recent collections in Colorado and Wyoming (Table 1). In North America, the family Diopsidae is represented by two species, S. subbifasciata and S. brevicornis. Feijen’s (1989) revision provides an excellent discussion of the family; unraveling the early synonymy, misspellings and historic misidentifications. He provided illustrations of the morphological characters of these species, a diagnostic key and listed examined material by states. Recent and past collection records show that specimens of S. subbifasciata are few and widely dispersed in Rocky Mountain states. We hypothesize that the unique Yellowstone habitat contains many warm springs and streams that may provide diopsids with protection from low winter temperatures and strong prairie winds. These flies are known to be poor fliers (Lavigne, 1962), but warm springs may provide good protection until adults could emerge in spring and disperse in summer. This behavior is consistent with that described for the closely related S. brevicornis (Flint, 1956; Hochberg-Stasny, 1985) and the geographically distant, but also closely related S. hearseiana Westwood from Bangladesh and India (Feijen, 1989). We do not know how they survive winters in northeastern Colorado unless they find protection in rock crevices, under rocks or wide bark of the few plains cottonwoods (Populus sargentii Dode) along the banks (Flint 1955, Lavigne, 1962) of Spottlewood Creek.

Previous experience matters in the stalk-eyed fly Teleopsis dalmanni

Previous experiences can play a significant role in determining future behaviors. Winner and loser effects, where the outcome of previous aggressive encounters influences the behavioral approach to and outcomes of future conflicts, have been documented in many taxa and illustrate this phenomenon. These effects are prevalent in species that interact frequently because modulation of these potentially costly social interactions may influence fitness. Stalk-eyed flies of the dimorphic species Teleopsis dalmanni engage in frequent fights over food resources, as well as over access to harems of females, with larger males typically prevailing when size disparities exist. However, whether and how prior experience influences fighting decisions and outcomes remains unexplored. To test for winner and loser effects in stalk-eyed flies, sexually mature flies were paired in size-mismatched dyads to establish winning and losing experiences. After their first contest, the flies were paired with size-matched individuals and allowed to interact. We determined whether an initial winning or losing experience significantly altered the outcome probabilities in the second size-matched encounter. Initial winning experience did not significantly affect the second interaction, providing no evidence for a winner effect. However, initial losers were significantly more likely to lose a subsequent interaction which provides evidence for a loser effect in stalk-eyed flies. In addition, smaller males experienced an increased probability of losing their second interaction regardless of prior winning or losing experience. This effect was not seen in large males. Our data suggest that the loser effects we observed, which were more pronounced in small males, could result from the energetic costs of fighting that they were less able to absorb than large males.

Compensation for exaggerated eye stalks in stalk-eyed flies (Diopsidae)

1. Exaggerated male ornaments often are hypothesised to increase predation risk due to reduced locomotor performance, yet empirical evidence supporting this proposition is equivocal. In part, current costs of ornaments may be difficult to detect in nature due to the evolution of compensatory mechanisms that offset detrimental effects. 2. The exaggerated eye stalks of male stalk-eyed flies increase their moment of inertia compared with females, yet males do not suffer a flight performance decrement. We tested for evidence of compensation within seven species of stalk-eyed flies, examining eyespan and wing size in four dimorphic and three monomorphic species. 3. We found that, within species, males had larger wings than females in two species dimorphic for eyespan but not in any monomorphic species. In males of the dimorphic species, there were positive relationships between relative eyespan and relative wing area, indicating compensation, whereas there were no such relationships in females of the dimorphic species or in either males or females of the monomorphic species. 4. We propose that examining compensatory abilities relative to ornament size is a powerful way to test for costs of ornaments in correlational and experimental studies.

The Enhancer of split complex arose prior to the diversification of schizophoran flies and is strongly conserved between Drosophila and stalk-eyed flies (Diopsidae)

BackgroundIn Drosophila, the Enhancer of split complex (E(spl)-C) comprises 11 bHLH and Bearded genes that function during Notch signaling to repress proneural identity in the developing peripheral nervous system. Comparison with other insects indicates that the basal state for Diptera is a single bHLH and Bearded homolog and that the expansion of the gene complex occurred in the lineage leading to Drosophila. However, comparative genomic data from other fly species that would elucidate the origin and sequence of gene duplication for the complex is lacking. Therefore, in order to examine the evolutionary history of the complex within Diptera, we reconstructed, using several fosmid clones, the entire E(spl)-complex in the stalk-eyed fly, Teleopsis dalmanni and collected additional homologs of E(spl)-C genes from searches of dipteran EST databases and the Glossina morsitans genome assembly.ResultsComparison of the Teleopsis E(spl)-C gene organization with Drosophila indicates complete conservation in gene number and orientation between the species except that T. dalmanni contains a duplicated copy of E(spl)m5 that is not present in Drosophila. Phylogenetic analysis of E(spl)-complex bHLH and Bearded genes for several dipteran species clearly demonstrates that all members of the complex were present prior to the diversification of schizophoran flies. Comparison of upstream regulatory elements and 3' UTR domains between the species also reveals strong conservation for many of the genes and identifies several novel characteristics of E(spl)-C regulatory evolution including the discovery of a previously unidentified, highly conserved SPS+A domain between E(spl)mγ and E(spl)mβ.ConclusionIdentifying the phylogenetic origin of E(spl)-C genes and their associated regulatory DNA is essential to understanding the functional significance of this well-studied gene complex. Results from this study provide numerous insights into the evolutionary history of the complex and will help refine the focus of studies examining the adaptive consequences of this gene expansion.

Screening Upland Varieties of NERICA and its Parents for Resistance to Stalk-eyed Fly, Diopsis sp. (Diptera, Diopsidae) in Benin

Screening Upland Varieties of NERICA and its Parents for Resistance to Stalk-eyed Fly, Diopsis sp. (Diptera, Diopsidae) in Benin

Wing size, wing shape and sexual dimorphism in eye-span in stalk-eyed flies (Diopsidae)

Wing size, wing shape and sexual dimorphism in eye-span in stalk-eyed flies (Diopsidae)

No Detectable Fertility Benefit from a Single Additional Mating in Wild Stalk-Eyed Flies

BackgroundMultiple mating by female insects is widespread, and the explanation(s) for repeated mating by females has been the subject of much discussion. Females may profit from mating multiply through direct material benefits that increase their own reproductive output, or indirect genetic benefits that increase offspring fitness. One particular direct benefit that has attracted significant attention is that of fertility assurance, as females often need to mate multiply to achieve high fertility. This hypothesis has never been tested in a wild insect population.Methodology/Principal FindingsFemale Malaysian stalk-eyed flies (Teleopsis dalmanni) mate repeatedly during their lifetime, and have been shown to be sperm limited under both laboratory and field conditions. Here we ask whether receiving an additional mating alleviates sperm limitation in wild females. In our experiment one group of females received a single additional mating, while a control group received an interrupted, and therefore unsuccessful, mating. Females that received an additional mating did not lay more fertilised eggs in total, nor did they lay proportionately more fertilised eggs. Female fertility declined significantly through time, demonstrating that females were sperm limited. However, receipt of an additional mating did not significantly alter the rate of this decline.Conclusions/SignificanceOur data suggest that the fertility consequences of a single additional mating were small. We discuss this effect (or lack thereof), and suggest that it is likely to be attributed to small ejaculate size, a high proportion of failed copulations, and the presence of X-linked meiotic drive in this species.

Germline transformation of the stalk-eyed fly, Teleopsis dalmanni

BackgroundStalk-eyed flies of the family Diopsidae have proven to be an excellent model organism for studying the evolution of ornamental sexual traits. In diopsid flies the eyes and antennae are borne at the end of lateral head projections called 'eye-stalks'. Eyespan, the distance between the eyes, and the degree of sexual dimorphism in eyespan vary considerably between species and several sexually dimorphic species show sexual selection through female mate preference for males with exaggerated eyespan. Relatively little is known about the molecular genetic basis of intra- or inter-species variation in eyespan, eye-stalk development or growth regulation in diopsids. Molecular approaches including comparative developmental analyses, EST screening and QTL mapping have identified potential candidate loci for eyespan regulation in the model species Teleopsis dalmanni. Functional analyses of these genes to confirm and fully characterise their roles in eye-stalk growth require the development of techniques such as germline transformation to manipulate gene activity in vivo.ResultsWe used in vivo excision assays to identify transposon vector systems with the activity required to mediate transgenesis in T. dalmanni. Mariner based vectors showed no detectable excision while both Minos and piggyBac were active in stalk-eyed fly embryos. Germline transformation with an overall efficiency of 4% was achieved using a Minos based vector and the 3xP3-EGFP marker construct. Chromosomal insertion of constructs was confirmed by Southern blot analysis. Both autosomal and X-linked inserts were recovered. A homozygous stock, established from one of the X-linked inserts, has maintained stable expression for eight generations.ConclusionsWe have performed stable germline transformation of a stalk-eyed fly, T. dalmanni. This is the first transgenic protocol to be developed in an insect species that exhibits an exaggerated male sexual trait. Transgenesis will enable the development of a range of techniques for analysing gene function in this species and so provide insight into the mechanisms underlying the development of a morphological trait subject to sexual selection. Our X-linked insertion line will permit the sex of live larvae to be determined. This will greatly facilitate the identification of genes which are differentially expressed during eye-stalk development in males and females.

A review of stalk-eyed fruit flies (Diptera: Tephritidae: Trypetinae)

Species of stalk-eyed fruit flies of the genera Pelmatops Enderlein and Pseudopelmatops Shiraki are reviewed and discussed; a key to the two genera and eight species is given. Pelmatops tangliangi Chen sp.nov., Pseudopelmatops indiaensis Chen sp.nov. and Pseudopelmatops yunnanensis Chen sp.nov. from the Oriental Region are described and illustrated.

Comparative Genomic Hybridization (CGH) reveals a neo-X chromosome and biased gene movement in stalk-eyed flies (genus Teleopsis).

Chromosomal location has a significant effect on the evolutionary dynamics of genes involved in sexual dimorphism, impacting both the pattern of sex-specific gene expression and the rate of duplication and protein evolution for these genes. For nearly all non-model organisms, however, knowledge of chromosomal gene content is minimal and difficult to obtain on a genomic scale. In this study, we utilized Comparative Genomic Hybridization (CGH), using probes designed from EST sequence, to identify genes located on the X chromosome of four species in the stalk-eyed fly genus Teleopsis. Analysis of log2 ratio values of female-to-male hybridization intensities from the CGH microarrays for over 3,400 genes reveals a strongly bimodal distribution that clearly differentiates autosomal from X-linked genes for all four species. Genotyping of 33 and linkage mapping of 28 of these genes in Teleopsis dalmanni indicate the CGH results correctly identified chromosomal location in all cases. Syntenic comparison with Drosophila indicates that 90% of the X-linked genes in Teleopsis are homologous to genes located on chromosome 2L in Drosophila melanogaster, suggesting the formation of a nearly complete neo-X chromosome from Muller element B in the dipteran lineage leading to Teleopsis. Analysis of gene movement both relative to Drosophila and within Teleopsis indicates that gene movement is significantly associated with 1) rates of protein evolution, 2) the pattern of gene duplication, and 3) the evolution of eyespan sexual dimorphism. Overall, this study reveals that diopsids are a critical group for understanding the evolution of sex chromosomes within Diptera. In addition, we demonstrate that CGH is a useful technique for identifying chromosomal sex-linkage and should be applicable to other organisms with EST or partial genomic information.

Sequential analysis of aggressive interactions in the stalk-eyed fly Teleopsis dalmanni

Understanding the mechanisms and determinants of conflict resolution is of great theoretical and practical importance because the outcome of contests between males over limited resources such as mates, territories, and food has profound fitness consequences. Despite the large literature on the theory of conflict resolution, relatively few empirical studies explicitly test predictions related to contest structure for these models. In sexually dimorphic species of stalk-eyed flies (Diopsidae), males engage in characteristic aggressive interactions over both females and food resources. We used sequential analysis of aggressive interactions between dyads of male stalk-eyed flies to investigate patterns of escalation, behavioral matching, and physical contact in order to distinguish between three common models of conflict resolution: the sequential assessment model, the cumulative assessment model, and the energetic war of attrition. Stalk-eyed flies were shown to engage in both low- and high-intensity behaviors during interactions with patterns of escalation and no de-escalation. Aggressive interactions did not demonstrate behavioral matching between winners and losers. Stalk-eyed flies also escalated to behaviors that included physical contact without injuries. Our results provide support for the sequential assessment model based on patterns of escalation with no de-escalation, behavioral mismatching, and behaviors which include physical contact but no injuries.

Low inbreeding depression in a sexual trait in the stalk-eyed fly Teleopsis dalmanni

The genic capture hypothesis implies that the expression of sexual ornaments largely depends on genes affecting resource acquisition and use. The ornaments should thus show high degree of directional dominance typical of life-history traits, and conse- quently, they should be severely affected by inbreeding. Here we investigated the effect of inbreeding on a sexual ornament (male eyespan) in stalk-eyed fly, Teleopsis dalmanni. For comparison, we also measured inbreeding depression in non-sexual morphological traits: female eyespan as well as wing and thorax lengths in both sexes. Both eyespan, and other morphological traits we measured, showed significant inbreeding depression. In accord with predictions of genic capture hypothesis, male eyespan did decrease under inbreeding significantly more than female eyespan. However, the decline in male eyespan was fully explained by overall decline in body length. Moreover, the magnitude of inbreeding depression in male eyespan was considerably lower than that typically observed for life- histories; in fact, it fitted within the range typically characterizing morphological traits. We therefore conclude that our results provide weak support for genic capture hypothesis.

Gender differences in survival and antipredatory behavior in stalk-eyed flies

Exaggerated eye span of stalk-eyed flies is a classic example of the evolution of an extravagant male ornament resulting from sexual selection. Increased male eye span may entail costs associated with production and/or maintenance, including potential locomotor costs that may increase predation risk. However, behavioral responses by individuals may alter the relationship between a morphological trait and performance, increasing expected overall fitness. Antipredator behavior and survival of male and female Teleopsis dalmanni were quantified during pairwise interactions between individual flies and an actively foraging, generalist arachnid predator (Phidippus audax). Male and female flies were compared under the assumption that female stalk length is closer to the optimum set by natural selection. There were significant differences in behaviors between the sexes, with males spending more time engaged in aggressive actions. Interestingly, males also exhibited increased survival relative to females. Within males, survivors did not differ from nonsurvivors in any of the morphological measures, including eye span, but there was a significant difference in abdomen bobbing, grooming, and flight. These results highlight the importance of behavior in the ability of stalk-eyed flies to effectively elude predators, but they do not support the hypothesis that male stalk-eyed flies suffer increased predation due to exaggerated eyestalks.

Wing shape, wing size, and sexual dimorphism in eye-span in stalk-eyed flies (Diopsidae)

The eyes of stalk-eyed flies (Diopsidae) are positioned at the end of rigid peduncles (‘stalks’) protruding laterally from the head. Eye-stalk length varies within the family and, in some species, varies between males and females. Larger eye-stalks in males result from sexual selection for longer stalks, a trait that increases male reproductive success. In the present study, we examined whether an increase in eye-stalk length results in an adjustment of wing size and shape to deal with the burden of bearing an exaggerated ‘ornament’. We compared wing morphology among ten species of stalk-eyed flies that differ in eye-span and the degree of sexual dimorphism. Mass-specific wing length differed between males and females in seven out of the ten species. Nondimensional wing shape parameters differed between the species (P < 0.001), but mostly did not differ between males and females of the same species. Dimorphism in eye-span closely correlated with dimorphism in wing length (r = 0.89, P < 0.001) and the correlation remained significant (r = 0.81, P = 0.006) after correcting for phylogenetic relationships. Once corrected for phylogenetic relatedness, the mass-specific wing length of males (but not females) was weakly correlated with mass-specific eye-span (r = 0.66, P = 0.042). We propose that the observed proportional increase in wing length associated with increased eye-span can facilitate aerial manoeuverability, which would otherwise be handicapped by the elevated moment of inertia imposed by the wider head.

Male eyespan and resource ownership affect contest outcome in the stalk-eyed fly, Teleopsis dalmanni

The dominant theory for the evolution of male sexual ornaments is that they act as signals of male quality used by females in their mate choice. But these traits may also be used in male–male competition. In stalk-eyed flies, male eyespan (the distance between the eyes) is already known to play an important role in female mate choice. We investigated the influence of eyespan on male aggression over control of lek mating sites, both under controlled conditions and from field observations. Eyespan positively affected the number of aggressive encounters between two males on a lek. There were more aggressive interactions between large-eyespan males compared with small-eyespan males, and large-eyespan males won proportionately more aggressive interactions. Lek site ownership also influenced the outcome of aggression but to a smaller degree than eyespan. In addition, higher resource value, the number of females on a lek, increased the chance of aggression. The outcome of aggression between males is the control of lek aggregation sites, and this had direct consequences for male reproductive success, as lek owners gained more matings at both dusk and dawn. The importance of male–male competition in shaping sexual selection in stalk-eyed flies is discussed.

Insects: Biggest! Littlest! (review)

Reviewed by: Insects: Biggest! Littlest! Elizabeth Bush Markle, Sandra . Insects: Biggest! Littlest!; illus. with photographs by Simon Pollard. Boyds Mills, 2009 32p. ISBN 978-1-59078-512-6 $16.95 R Gr. 2-4 The name Markle carries the promise of clarity and precision in text and photo illustration, a promise generally fulfilled in this primary-level exploration of insects notable for straying from the size norm. Some of the choices are fairly obvious—the pea aphid, "so little she could fit on the head of a pin," and the Raja Brooke birdwing butterfly, with a wingspan of nearly a foot. Markle, however, expands her definition of "big" and "little" beyond length; outsized body parts get some attention (jaws on male stag beetles, eye stalks on male stalk-eyed flies) as do insects, such as honeybees and carpenter ants, that gang up in really big groups for protection and predation. An appended note indicates that the text has been developed to support national science standards that prescribe examination of animal structures and behaviors relating to growth, survival, and reproduction, making this a bonus to classroom teachers seeking high-quality material clearly aligned to teaching standards. The paucity of visual clues to the relative size of each little beastie—Pollard's glorious close-ups rarely offer a frame of reference for comparison—is an unfortunate drawback, but Markle does at least note the measurements of the insects, so kids who are willing or encouraged to get out their rulers can bring a hands-on dimension to their armchair nature study. A glossary and brief list of children's books and websites is included. Copyright © 2009 The Board of Trustees of the University of Illinois

Eyespan reflects reproductive quality in wild stalk-eyed flies

Handicap models of sexual selection propose that females use male sexual ornaments as a cue in mate choice because they reflect commodities that increase female fitness, either directly or indirectly. In contrast to studies on vertebrates, most investigations of ornaments in insects and other invertebrate taxa have been conducted under laboratory conditions. There is a pressing need to address questions relating to sexual signalling of quality in natural populations, as the arbitrary and uniform environments found in the laboratory fail to reflect the world under which animals have evolved. We investigated associations between male ornaments (exaggerated eyespan), attractiveness, and reproductive quality in a wild population of the sexually ornamented stalk-eyed fly, Teleopsis dalmanni. We also explored the relationship between eyespan and reproductive quality in females to evaluate the potential for sexually antagonistic selection on eyespan. We show that eyespan is a generic correlate of reproductive quality, acting as a reliable mirror of variation in reproductive fitness in both sexes. Our findings suggest that male ornaments signal commodities that are of interest to females in the natural environment in which they, and mate preferences for them, have evolved. In addition, the covariance between female eyespan and reproductive output suggests that the former may be a reliable cue of quality in its own right. Our data provide important insights into the evolutionary forces that shape the evolution of exaggerated eyespan in wild populations of this species.

Genomic analysis of a sexually-selected character: EST sequencing and microarray analysis of eye-antennal imaginal discs in the stalk-eyed fly Teleopsis dalmanni (Diopsidae).

BackgroundMany species of stalk-eyed flies (Diopsidae) possess highly-exaggerated, sexually dimorphic eye-stalks that play an important role in the mating system of these flies. Eye-stalks are increasingly being used as a model system for studying sexual selection, but little is known about the genetic mechanisms producing variation in these ornamental traits. Therefore, we constructed an EST database of genes expressed in the developing eye-antennal imaginal disc of the highly dimorphic species Teleopsis dalmanni. We used this set of genes to construct microarray slides and compare patterns of gene expression between lines of flies with divergent eyespan.ResultsWe generated 33,229 high-quality ESTs from three non-normalized libraries made from the developing eye-stalk tissue at different developmental stages. EST assembly and annotation produced a total of 7,066 clusters comprising 3,424 unique genes with significant sequence similarity to a protein in either Drosophila melanogaster or Anopheles gambiae. Comparisons of the transcript profiles at different stages reveal a developmental shift in relative expression from genes involved in anatomical structure formation, transcription, and cell proliferation at the larval stage to genes involved in neurological processes and cuticle production during the pupal stages. Based on alignments of the EST fragments to homologous sequences in Drosophila and Anopheles, we identified 20 putative gene duplication events in T. dalmanni and numerous genes undergoing significantly faster rates of evolution in T. dalmanni relative to the other Dipteran species. Microarray experiments identified over 350 genes with significant differential expression between flies from lines selected for high and low relative eyespan but did not reveal any primary biological process or pathway that is driving the expression differences.ConclusionThe catalogue of genes identified in the EST database provides a valuable framework for a comprehensive examination of the genetic basis of eye-stalk variation. Several candidate genes, such as crooked legs, cdc2, CG31917 and CG11577, emerge from the analysis of gene duplication, protein evolution and microarray gene expression. Additional comparisons of expression profiles between, for example, males and females, and species that differ in eye-stalk sexual dimorphism, are now enabled by these resources.

The Evolution of Extraordinary Eyes: The Cases of Flatfishes and Stalk-eyed Flies

The history of life is an unbroken stream of evolution stretching over 3.5 billion years. In order to study it—and in order to describe it—it must be carved into episodes. If scientists want to understand the origin, say, of bats, they do not run experiments to test a hypothesis about how DNA first evolved on the early Earth. They do not do research on the transition from single-celled protozoans to the first animals 600 million years ago. Likewise, they do not get bogged down with bat evolution after bats first evolved— how, for example, bats spread around the world and how they coevolved with their prey. There is only so much time in the day. Science writers follow the same rules to describe evolution. A newspaper article on the evolution of bats must focus only on that brief episode of life’s history. Let its scope grow too large, and it will be too big for a book— or a shelf of books. This simple necessity can, unfortunately, give people the wrong impression about evolution. We tend to picture evolution as a series of isolated milestones. Once some particular trait evolves, we may assume that evolution simply stops. The history of eyes is particularly vulnerable to this illusion. Consider, for example, a masterful paper entitled, “Evolution of the vertebrate eye: opsins, photoreceptors, retina, and eye cup,” published by Trevor Lamb of Australian National University and his colleagues in the December 2007 issue of Nature Reviews Neuroscience (Lamb et al. 2007). “Here,” Lamb and his co-authors announce, “we review a wide range of findings that capture glimpses of the gradations that appear to have occurred during eye evolution, and provide a scenario for the unseen steps that have led to the emergence of the vertebrate eye.” They end their review with the emergence of the vertebrate eye. Of course, Lamb et al. (2007) do not mean to imply that the evolution of vertebrate eyes ceased after they first emerged. But their focus is not on what happened afterwards. Figuring out how a patch of light-sensitive receptors evolved into a camera-like imaging system shared by 40,000-odd species of vertebrates is certainly an important thing to do, and it is a job that will fill many scientists’ entire careers. But when the first full-blown vertebrate eyes emerged in some primitive fishes half a billion years ago, the evolution of the vertebrate eye did not stop. The eyes of every vertebrate alive today are different in some important ways from those early eyes. In some cases, the transformation has been exquisitely subtle. But in others, it has been so extreme as to be quite striking. In this essay, I will look at two animals in which evolution has radically reworked a “standard” kind of eye: flatfishes and stalk-eyed flies. In both cases, eyes have moved far from their original position on the head. But flatfishes and stalk-eyed flies are not just freakish codas on the symphony of evolution. Instead, they are remarkable illustrations of some of the most powerful forces shaping all life, weird or otherwise. Flatfishes—such as flounder, turbot, and plaice—are among the most striking animals in the sea. They spend much of their adult life sideways, hugging the sea floor where they lie in wait to ambush smaller fish. Their anatomy and DNA both reveal that they belong to the most diverse radiation of vertebrates today, known as the teleosts. Teleosts include most of the fishes we are most familiar with, such as goldfish and trout. In many respects, flatfishes have a standard teleost body plan. But as they Evo Edu Outreach (2008) 1:487–492 DOI 10.1007/s12052-008-0089-9