Convergence in feeding posture occurs through different genetic loci in independently evolved cave populations of Astyanax mexicanus

Abstract

When an organism colonizes a new environment, it needs to adapt both morphologically and behaviorally to survive and thrive. Although recent progress has been made in understanding the genetic architecture underlying morphological evolution, behavioral evolution is poorly understood. Here, we use the Mexican cavefish, Astyanax mexicanus, to study the genetic basis for convergent evolution of feeding posture. When river-dwelling surface fish became entrapped in the caves, they were confronted with dramatic changes in the availability and type of food source and in their ability to perceive it. In this setting, multiple independent populations of cavefish exhibit an altered feeding posture compared with their ancestral surface forms. We determined that this behavioral change in feeding posture is not due to changes in cranial facial morphology, body depth, or to take advantage of the expansion in the number of taste buds. Quantitative genetic analysis demonstrates that two different cave populations have evolved similar feeding postures through a small number of genetic changes, some of which appear to be distinct. This work indicates that independently evolved populations of cavefish can evolve the same behavioral traits to adapt to similar environmental challenges by modifying different sets of genes.T he colonization of caves is an extreme example of a species entering a new environment. Unique attributes of caves relative to the surface environment include darkness, high humidity, relatively constant temperature, absence of predators, and scarcity of food. Under these circumstances, many species of cave animals have evolved a suite of similar traits, including constructive traits such as heightened sensory systems and regressive traits such as loss of pigmentation and reduction in eye morphology (1). To study the evolution of cave-specific traits, we have focused on Astyanax mexicanus, the Mexican cavefish. A. mexicanus exists in two forms, a cave-dwelling form and a river-dwelling surface form. Importantly, these forms are still interfertile (2), allowing one to take a genetic approach using quantitative trait loci (QTL) analysis for the mapping of cave traits. Furthermore, there are multiple, independently evolved cave populations (3-7) that in many cases have evolved similar traits, allowing for the study of convergent evolution.Populations of cave organisms have often been the subjects of studies on convergence. For example, loss of pigmentation evolved via disruptions in the first step of the melanin synthesis pathway in multiple species of cave organisms (8). Similarly, a decrease in the levels of melanin synthesis arose in multiple cave populations of A. mexicanus through different mutations in the same genes (9, 10). In contrast, crosses between multiple cave populations of A. mexicanus result in embryonic hybrid fish with larger, functional eyes, indicating that evolution of this trait is controlled by different genetic loci in different cave populations (2, 11).Among the most intriguing and least und...

The Evolution of Sensory Adaptation in Astyanax mexicanus

“…Because cavefish show enhanced tastebud numbers mostly at the epidermis of the lower jaw facing the bottom of the pool, it was once suggested that these gustatory structures were linked to bottom-feeding posture (Schemmel, 1980), as cavefish feed at the bottom with their anteroposterior body axis oriented at a ~45° angle to the substrate. In contrast, when surface fish feed at the bottom, they orient their anteroposterior body axis perpendicular to the bottom and cannot stabilize their body posture in darkness; however, a series of genetic analyses using F 2 hybrids showed no correlation between bottom-feeding posture and these gustatory traits, as well as other cranial morphologies, suggesting that this bottom-feeding posture is instead based upon changes to the central nervous system (Kowalko et al, 2013b). Furthermore, QTL mapping revealed that the QTL for this bottom-feeding posture is not associated with the shh locus, revealing that these traits evolved without shh mutation; conversely, tastebud number is controlled by an shh overexpression (Figure 13.3).…”

“…The molecular pathways leading to VAB and (Yoshizawa et al, 2012;Kowalko et al, 2013b) Eye size Amino acid sensing Taste bud number (Protas et al, 2008) Eye size VAB EO SN number Feeding angle FIGURE 13.3 See legend next page associated changes in SN number and eye size may be distinct (Yoshizawa et al, 2012), but the correlations among these traits suggest that the reduction of eye size provides more space for SN at the eye orbit and therefore promotes VAB. Alternatively, multi-trait QTL clustering (i.e., where genes that regulate each different trait form a cluster in a confined area within the genome) may link suites of traits that are necessary for adaptation.…”

“…Colored bars represent approximate position of QTL for eye size, chemical (amino acid) sensing ability, tastebud number, VAB level, EO SN number, and feeding angle (Kowalko et al, 2013b;Protas et al, 2008;Yoshizawa et al, 2012). Many zebrafish mutants harbor defects in physiology and/or morphology.…”

Multiple evolutionary origins of Australian soil-burrowing cockroaches driven by climate change in the Neogene

“…Some have argued that evolution is fundamentally stochastic and unpredictable [3], while others have proposed that constraints commonly limit available phenotypic options, leading to parallelism and predictability [4]. Although parallel genotypic adaptation has been demonstrated across a diverse range of taxa at the intraspecific level [5][6][7][8][9][10][11], the widespread occurrence of parallel evolution across a clade has only rarely been shown [12,13]. The potential role of environmental change in driving parallel evolution also remains poorly understood [14].…”

A mutation in the enzyme monoamine oxidase explains part of the Astyanax cavefish behavioural syndrome

“…In particular, Astyanax cave morphs have lost their eyes and their pigmentation, and they have also lost sleep 12,13 , schooling 14,15 and hierarchical aggressive behaviour [16][17][18] . On the other hand, they have gained adaptive behaviours such as attraction to vibrations 19 , increased exploratory [20][21][22][23][24] and food searching behaviour 17 , and a special feeding posture 25,26 . This is sometimes referred to as 'the cavefish behavioural syndrome'.…”