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The forces driving regression of biologically functionless traits remain disputed. There is ongoing debate regarding whether selection, as opposed to disuse and neutral mutations, is involved in this process. Cave species are of particular relevance for study in this regard because in continuous darkness all traits that depend on information from light, such as eyes, dark pigmentation and certain behaviours, abruptly lose their function. Recently, strong selection driving reduction has again been proposed, which relied on modelling analyses based on assumptions such as immigration of surface alleles into the cave forms or no fitness difference existing between Astyanax surface and cave fish. The validity of these assumptions, often applied to reject neutral processes in functionless traits, is questioned in this review. Morphological variation in a trait resulting from genetic variability is typical of biologically functionless traits and is particularly notable in phylogenetically young cave species. It is the most evident indicator of loss of selection, which normally enforces uniformity to guarantee optimal functionality. Phenotypic and genotypic variability in Astyanax cave fish eyes does not derive from genetic introgression by the surface form, but from regressive mutations not being eliminated by selection. This matches well with the principles of Kimura’s neutral theory of molecular evolution.

The retina has a very high energy demand but lacks an internal blood supply in most vertebrates. Here we explore the hypothesis that oxygen diffusion limited the evolution of retinal morphology by reconstructing the evolution of retinal thickness and the various mechanisms for retinal oxygen supply, including capillarization and acid-induced haemoglobin oxygen unloading. We show that a common ancestor of bony fishes likely had a thin retina without additional retinal oxygen supply mechanisms and that three different types of retinal capillaries were gained and lost independently multiple times during the radiation of vertebrates, and that these were invariably associated with parallel changes in retinal thickness. Since retinal thickness confers multiple advantages to vision, we propose that insufficient retinal oxygen supply constrained the functional evolution of the eye in early vertebrates, and that recurrent origins of additional retinal oxygen supply mechanisms facilitated the phenotypic evolution of improved functional eye morphology.

Processes of regression and rudimentation are deeply involved in the evolution of life and are as important as constructive evolution. They occur in every taxonomic group and concern morphological, behavioural, as well as physiological traits. For example, whales have reduced their hind legs and the pelvic girdle. The ratite birds have convergently abandoned the ability to fly and exhibit reduced wings and sternal carina. In addition, the delicate feather structure is broken down. In the Pacific island of Tahiti, where no insectivore bats exist, noctuid moths have lost the acoustic startle response. Even the gustatory system may selectively lose taste components (e.g. sweet in cats; bitter, sweet, and umami in penguins; or umami in the giant panda after changing their diet during evolution). However, from the view of human beings relying on sight as the dominant sense, the most bizarre and striking examples for rudimentation—often also characterized as degeneration or regression of traits—are provided by the loss of eyes and dark pigmentation in species living in the continuous absolute darkness of subterranean habitats like caves.

One epigean and five cave populations of Astyanax fasciatus were compared with respect to egg and embryo size as well as yolk volume 12 h and 24 h after fertilization. All cave fish have significantly bigger eggs and embryos with more yolk than the epigean ancestor. There are no differences in the chemical composition of cave and surface fish eggs. The genetic analysis of yolk content reveals an additive polygenic mode of inheritance. Zusammenfassung Dotterreichere Eier bei unterirdisch lebenden Astyanax fasciatus (Characidae, Pisces) Eine oberirdische und funf unterirdische Populationen von Astyanax fasciatus wurden in Hinsicht auf Ei- und Embryogrose und auf Dottervolumen 12 h und 24 h nach der Befruchtung unter-sucht. Alle Hohlenfische haben signifikant grosere Eier und Embryonen mit mehr Dotter als der oberirdische Verwandte. Dagegen bestehen keine Unterschiede in der chemischen Zusammenset-zung der Eier ober- und unterirdischer Fische. Die genetische Analyse zeigt, das das Dottervolumen additiv polygen vererbt wird.

The early morphogenesis of the lens and the expression of the γs-crystallin gene was studied in epigean Astyanax fasciatus and its cave-dwelling derivative. At early stages, the lens of the cave fish develops in a way that is similar to the epigean form. Later, the developmental timing is delayed and growth ceases in the cave-fish lens. With the beginning of cytodifferentiation, the development of the lens breaks down. Crystallin lens fibres are not produced at any time and the γs-crystallin gene, which is transcribed during a limited period in the lens of epigean fishes, is not active in cave specimens. This study confirms earlier immunofluorescence observations that demonstrated the lack of crystallin proteins in the cave-fish lens, but is in contrast to results on the blind mole rat, which showed a persistence of functioning crystallins in the degenerated lens of this species. The significance of developmental constraints in regressive evolution is discussed. Zusammenfassung Entwicklungsbedingte Beschrankungen in der regressiven Evolution: Untersuchungen zur Expression des γs-Krystallin Gens in der Linsenentwicklung des Hohlenfisches Astyanax fasciatus (Teleostei, Characidae) durch in situ Hybridisierung Die fruhe Morphogenese der Linse und die Expression des γs-Kristallin Gens wurden in dem oberirdischen Fisch Astyanax fasciatus und seiner Hohlenform untersucht. In fruhen Stadien entwickelt sich die Linse des Hohlenfischauges ahnlich wie die der oberirdischen Form. Es setzt jedoch bald eine Verzogerung in der Entwicklung der Hohlenfischlinse ein, die spater zum Entwicklungsstillstand fuhrt. Mit Beginn der Zelldifferenzierung bricht die Linsenentwicklung ab. Kristalline Linsenfasern werden zu keinem Zeitpunkt entwickelt und die mRNA des γs-Kristallin Gen, das in der oberirdischen Form wahrend eines begrenzten Zeitraumes exprimiert wird, kann in der Linse der Hohlenfische zu keiner Zeit nachgewiesen werden. Diese Untersuchungen bestatigen fruhere immunohistochemische Arbeiten, in denen das Fehlen von Kristallin-Proteinen in der Hohlenfischlinse nachgewiesen wurde. Sie stehen jedoch im Gegensatz zu Untersuchungen an dem Blindmull Spalax ehrenbergi, in dessen degenerierten Augen funktionell intakte Kristalline nachgewiesen wurden.

The West Indian Ophidiiform fish are characterized by the occurrence of several troglobitic species. They are Ogilbia (= Typhliasina) pearsei (Yucatan), Lucifuga subterraneus, L. dentatus and L. simile (Cuba), and L. spelaeotes (Bahama Islands). The surface relatives, e. g. Ogilbia spp., prefer lightpoor zones. This is shown by a large lens and a retina almost exclusively consisting of rods. L. dentatus, L. subterraneus, and O. pearsei possess extremely reduced eyes. The eye of L. spelaeotes has morphologically an intermediate position. In correlation to varying eye size a dif­ ferent number of rods may be developed. Furthermore in some specimens the lens starts de­ generating. Contrary to the extremely reduced cave forms all specimens of L. spelaeotes can still perceive light with their eyes. The different degrees of reduction in the West Indian Ophidiiform cave fish probably reflect varying phylogenetic ages. A possible date of origin of L. spelaeotes could be at the beginning or the end of the last glaciation. The eyes of neonate individuals of the live-bearing L. dentatus and O. pearsei possess a lens and a retina rudiment. No fundamental structural and histological differences between both species were found at this stage.

Two hypotheses exist to explain ontogenetic eye reduction in Astyanax cave fish: first, after lens induction by the primordial eye cup, the lens plays the role of a central regulator of eye and retina regression or, second, the retina itself is an independent unit of eye development. A comparative study of five blind cave fish populations and their surface sister form was performed to investigate the differences of ontogenetic eye regression between the cave populations during different stages of development. The study revealed that, in addition to the initial formation of smaller primordia, eye regression is also caused during later ontogeny by different relative growth and specific histological characteristics. Whereas the cave fish lens never properly differentiates, the regressive process of the retina is transitorily interrupted by ongoing differentiation. In the newly-discovered Molino cave population, even visual cells with well-organized outer segments develop, which are secondarily reduced at a later ontogenetic stage. This result shows that the retina and lens are independent developmental units within the eye ball. Presumably, the genetic systems responsible for both show independent inheritance, which is also corroborated by hybrids of F2-crosses between the cave and surface fish, in which lens and retina development do not correlate. During ontogeny, the eye size differs between the cave populations. In Pachon cave fish, the relatively large eye size correlates with an ancient introgression from a surface population, which may have delayed eye regression. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92, 287–296.

Regressive evolution, the reduction or total loss of non-functional characters, is a fairly common evolutionary phenomenon in subterranean taxa. However, the genetic basis of regressive evolution is not well understood. Here we investigate the molecular evolution of the eye pigment genecinnabarin several independently evolved lineages of subterranean water beetles using maximum likelihood analyses. We found that in eyeless lineagescinnabarhas an increased rate of sequence evolution, as well as mutations leading to frame shifts and stop codons, indicative of pseudogenes. These results are consistent with the hypothesis that regressive evolution of eyes proceeds by random mutations, in the absence of selection, that ultimately lead to the loss of gene function in protein-coding genes specific to the eye pathway.

The early morphogenesis of the degenerate eyes of the Mexican cave fish Astyanax fasciatus and of its conspecific epigean ancestor has been studied comparatively using light- and electron-microscopical techniques; the transcription of the opsin gene has been analysed during early ontogeny in both populations by in situ hybridization. The opsin protein is an integral component of the disk membranes of the photoreceptor cells. In epigean specimens, its expression is correlated with the beginning of outer segment formation on the third day of development. Morphogenesis of the cave fish eye is similar to that of the epigean eye until end of the third day. However, eye growth and morphogenesis of the retina are delayed and sporadic cell death occurs in all retinal layers at the beginning of the second day. Retinal cytodifferentiation breaks off at the point of outer segment formation. Cave specimens are not able to develop regular outer segments at any stage, but the opsin gene is nevertheless expressed in the outer nuclear layer of the developing retina for a limited period of time. On the basis of the comparative morphology and transcriptional studies of epigean and cave specimens, it is suggested that the eye regression of cave fish is primarily the result of mutations of developmental control genes and not of structural genes.

The genetic basis of vertebrate morphological evolution has traditionally been very difficult to examine in naturally occurring populations. Here we describe the generation of a genome-wide linkage map to allow quantitative trait analysis of evolutionarily derived morphologies in the Mexican cave tetra, a species that has, in a series of independent caves, repeatedly evolved specialized characteristics adapted to a unique and well-studied ecological environment. We focused on the trait of albinism and discovered that it is linked to Oca2, a known pigmentation gene, in two cave populations. We found different deletions in Oca2 in each population and, using a cell-based assay, showed that both cause loss of function of the corresponding protein, OCA2. Thus, the two cave populations evolved albinism independently, through similar mutational events.