Driven by the senses: support grows for the role of visual divergence in cichlid speciation

by Nicole M. Hourie, Scripps College [edited by Lars Schmitz as part of BIOL 167 “Sensory Evolution”, an upper division class at the W.M. Keck Science Department. Written for educational purposes only].

When an organism encounters different ecological niches, populations may undergo divergent selection tied to the requirements of each niche. When this occurs, reproductive isolation may take place, eventually resulting in the formation of distinct species (Van Valen, 1976). While this narrative of ecological speciation is well established and makes frequent appearances in biology textbooks, the selective forces that initiate this process are often quite challenging to determine (Maan, Seehausen, and Groothius, 2016). However, studies over the last decade have begun to shed light on the important role that sensory drive may play in speciation. Here I will dive deeper into how exposure to alternative sensory environments, with specific focus on visual conditions, may lead to divergent sensory adaptations and eventual speciation.

What do we already know?

We all know as living creatures that sensory perception is critically important for survival and reproduction. In addition, there are a variety of different sensory environments that animals can inhabit. Non-surprisingly then, there exists a large diversity in sensory systems across the animal kingdom, depending on various navigation, food detection, predator evasion, and mate selection requirements.

Perhaps the most abundant research involving the role of such sensory drive is focused on aquatic environments where heterogeneity in visual conditions is greatly pronounced by changes in water depth and turbidity (Maan, Seehausen, and Groothius, 2016). Cichlids are a family of fish that are known to be among the most species-rich within vertebrates, consisting of approximately 2,000 species (Kocher, 2004)! Certain cichlid lineages, such as haplochromines, have been subject to multiple adaptive radiations, making them a point of interest in speciation research (Salzburger et al., 2005). Previous studies have found that such radiations show considerable variation in color vision traits, which has been correlated to differing visual habitat and sexual selection (Boughman, 2002; Carleton et al., 2005; Maan et al., 2006; Seehausen et al., 2008; Miyagi et al., 2012).

The two haplochromine species that I will be paying special attention to are Pundamilia pundamilia and Pundamilia nyererei. These incipient sister species have reached a level in speciation where reproductive isolation has been mostly achieved, but occasional hybridization does occur (Seehausen, 2009). Both are known to inhabit Lake Victoria, a location in Africa where over 500 species of brightly colored cichlids have radiated over a short span of time (Fryer and Iles, 1972). However, P. nyererei lives at greater water depths than P. pundamilia and, therefore, encounters a very different visual environment (Seehausen 2009; Maan, Seehausen, and Groothius, 2016). In the turbid waters of Lake Victoria, light with short wavelengths, such as blue and violet, is absorbed rapidly while longer wavelength light, such as red and yellow, penetrates to greater water depths (Lythgoe, 1984). As a result, the deeper habitat of P. nyererei has a reddish/yellowish spectrum, as compared to the broad daylight spectrum that P. pundamilia experiences. This variation in photic environment has been associated with genetic differences between the two species, resulting in divergent color vision traits and male body color (Carleton et al., 2005). Previous research has found that, due to differences in color vision, P. pundamilia females prefer the jet blue coloration characteristic of P. pundamilia males, while P. nyererei females prefer the red coloration of P. nyererei males (Selz et al., 2014). Such findings demonstrate how sensory drive may play a vital role in the reproductive isolation of these cichlids (Figure 1).

Figure 1

Figure 1. Overview of how sensory drive has contributed to the population divergence and reproductive isolation of P. pundamilia and P. nyererei. Taken from “Sex, speciation, and fishy physics”. Understanding Evolution. University of California Museum of Paleontology. 02 May 2017, http://evolution.berkeley.edu/evolibrary/news/090301_cichlidspeciation.

Measuring fitness

Now that we’ve seen how differences in visual environment can influence sexual selection, let us ask how might it influence survival. A recent study conducted by Maan, Seehausen, and Groothuis addresses a key component of haplochromine speciation that had not yet been researched in terms of sensory drive – fitness. In order to initiate and sustain divergent populations, the adaptations selected for in a given niche most commonly convey some sort of fitness advantage (Maan, Seehausen, and Groothius, 2016). These researchers wanted to see if the adaptations forming in P. pundamilia and P. nyererei actually gave them a greater survival rate within their visual niche. To find out, they set up reciprocal transplant experiments in which groups of P. pundamilia and P. nyererei were reared in shallow light conditions and deep light conditions (Figure 2 & 3).  The shallow conditions were made to emulate the natural visual environment of P. pundamilia and the deep conditions resembled the natural visual environment of P. nyererei. In this way, experimenters were able to compare the survival rates between treatments.

Figure 2

Figure 2. Generalized schematic of the reciprocal transplant experimental set-up used by Maan, Seehausen, and Groothius to compare the effect of visual environment on the fitness of P. pundamilia and P. nyererei. Source: Nicole Hourie.

Figure 3

Figure 3. Males in light treatments – P. pundamilia (full brothers; top) and P. nyererei (full brothers; bottom) in shallow visual environment (left) and deeper visual environment (right). From Maan, Seehausen, and Groothius, 2016. Photos by D. Shane Wright.

What they found was that both P. pundamilia and P. nyererei did indeed have higher survival rates in the light environment that mimicked their natural habitat (Figure 4). This study therefore provides the first evidence suggesting that the differences in visual perception between these species convey a fitness advantage within the species’ niche. These findings further bolster the notions that 1) the differences in color vision are adaptive and 2) the differences in visual environment are a strong enough force to drive such divergence in visual properties. Not to mention, since the two species used are still in intermediate stages of speciation, the implication can be made that differing visual adaptations play a significant role in the initiation of population divergence.

Figure 4

Figure 4. Survival rate of F1 offspring of P. pundamilia, P. nyererei, and hybrids under light treatments simulating their natural visual environments of Lake Victoria. (Top six panels) Proportion of surviving offspring at 6 and 12 months in the shallow treatment (upper panels) and the deeper treatment (lower panels). Each line/symbol represents a different family. (Bottom two panels) Average proportion of surviving offspring across families. From Maan, Seehausen, and Groothius, 2016.

Let’s get complicated

Their study also compared the survival rates of hybrids in the two light conditions. Here the survival rates did not significantly differ between the visual environments. This makes sense since, in theory, the hybrid represents an intermediate of both parental species (Carleton et al., 2010). Another finding was that the survival rate of hybrids did not significantly differ from that of either parental species in their natural visual habitat. This complicates things a bit. This and previous work has attempted to identify visual environment as the driving force in the speciation of haplochromine cichlids by causing disruptive selection. If this were fully the case, we would expect hybrids to have a lower fitness than either parental species in their natural environment.

For instance, say we have a hybrid and P. nyererei living in the deep habitat treatment. Since P. nyererei has adapted color vision and pigmentation that best suits the light spectrum of deeper waters, we would expect P. nyererei to have a higher survival rate than the hybrid. Because actual results show that the hybrid had a survival rate similar to P. nyererei, we must now consider that differences in visual environment alone may not be enough to cause diverging populations (Maan, Seehausen, and Groothius, 2016). This is not to say that sensory drive does not contribute to speciation whatsoever. What it does mean is that sensory drive may work in conjunction with other ecological factors to facilitate population divergence.

Indeed, other studies have attempted to identify other adaptive divergences involved in the speciation between P. pundamilia and P. nyererei. For instance, a study conducted by Dijkstra, Seehausen, and Metcalfe implicated a divergence in metabolic efficiency and agonistic behavior between the two species as contributing to their speciation. They expected that P. nyererei males would experience a metabolic cost as a result of exhibiting more aggressive behavior (Dijkstra, Seehausen, and Metcalfe, 2013). However, results suggested the opposite – P. nyererei males used less oxygen (for a given body mass) during territorial interactions than P. pundamilia males. Researchers concluded that such findings imply that metabolic efficiency is an adaptation to reduce the cost associated with increased aggression (Dijkstra, Seehausen, and Metcalfe, 2013). However, their results also found that level of territorial aggressiveness did not differ between the two species when placed in social treatments, contradictory to other studies that have observed a heightened aggression in P. nyererei males. While this work hypothesizes that divergence in agonistic behavior and metabolic efficiency may play an important role in the rapid speciation of the haplochromine lineage, it is yet to be substantially supported.

What does this mean for future research?

Undeniably there is a large body of work that implicates sensory adaptations as a major factor of the rapid speciation in the haplochromine lineage. While Mann, Seehausen, and Groothius’s experiment supports the role of sensory drive in cichlid speciation, it also highlights that the entire picture may not yet be fully realized. Continued research must therefore be devoted to identifying any other contributing ecological factors that additionally influence speciation in cichlids.

 

References

Boughman, J. W., 2002 How sensory drive can promote speciation. Trends Ecol Evol 17(12), 571-577. (DOI 10.1016/S0169-5347(02)02595-8)

Carleton, K. L., Hofmann, C. M., Klisz, C., Patel, Z., Chircus, L. M., Simenauer, L. H., Soodoo, N., Albertson, R. C., Ser, J. R. 2010 Genetic basis of differential opsin gene expression in cichlid fishes. J Evolution Biol 24(3), 840-853. (DOI 10.1111/j.1420-9101.2010.01954)

Carleton, K. L., Parry, W. L., Bowmaker, J. K., Hunt, D. M., Seehausen, O. 2005 Colour vision and speciation in Lake Victoria cichlids of the genus Pundamilia. Mol Ecol. 14(14), 4341-53. (DOI 10.1111/j.1365-294X.2005.02735.x)

Dijkstra, P. D., Seehausen, O., Metcalfe, N. B. 2013 Metabolic divergence between sibling species of cichlids Pundamilia nyererei and Pundamilia pundamilia. J Fish Biol 82(6), 1975-89. (DOI 10.1111/jfb.12125)

Fryer, G., Iles, T. D. 1972. The cichlid fishes of the great lakes of Africa: their biology and evolution. (CA): Oliver and Boyde.

Kocher, T. 2004 Adaptive evolution and explosive speciation: the cichlid fish model. Nat Rev Genet 5, 288-298. (DOI 10.1038/nrg1316)

Lythgoe, J. N. 1984 Visual pigments and environmental light. Vision Res 24(11), 1539-50.

Maan, M. E., Hofker, K. D., van Alphen, J. J. M., Seehausen, O. 2006 Sensory drive in cichlid speciation. American Naturalist 167(6), 947-964. (DOI 10.1086/503532)

Maan, M. E., Seehausen, O., Groothius, T. G. G. 2016 Differential Survival between Visual Environments Supports a Role of Divergent Sensory Drive in Cichlid Fish Speciation. American Naturalist 189 (1), 78-85. (DOI 10.1086/689605)

Miyagi, R., Terai, Y., Aibara, M., Sugawara, T., Imai, H., Tachida, H., Mzighani, S. I., Okitsu, T., Wada, A., Okada, N. 2012 Correlation between nuptial colors and visual sensitivities tuned by opsins leads to species richness in sympatric Lake Victoria cichlid fishes. Mol Biol Evol 29(11), 3281-96. (DOI 10.1093/molbev/mss139)

Salzburger, W., Mack, T., Verheyen, E., Meyer, A. 2005 Out of Tanganyika: genesis, explosive speciation, key-innovations and phylogeography of the haplochromine cichlid fishes. BMC Evol Biol 5(17). (DOI 10.1186/1471-2148-5-17)

Seehausen, O. 2009 Progressive levels of trait divergence along a “speciation transect” in the Lake Victoria cichlid fish Pundamilia. in Butlin, R. K., Schluter, D., Bridle, J. R., eds. Speciatoion and patterns of diversity. Cambridge University Press, New York.

Seehausen, O., Terai, Y., Magalhaes, I. S. Carleton, K. L., Mrosso, H. D. J., Miyagi, R., van der Sluijs, I., Schneider, M. V., Maan, M. E., Tachida, H., Imai, H., Okada, N. 2008 Speciation through sensory drive in cichlid fish. Nature 455, 620-626. (DOI 10.1038/nature07285)

Selz, O. M., Pierotti, M. E. R., Maan, M. E., Schmid, C., Seehausen, O. 2014 Female preference for male color is necessary and sufficient for assortative mating in 2 cichlid sister species. Behav Ecol 25(3), 612-626. (DOI 10.1093/beheco/aru024)

Van Valen, L. 1976 Ecological Species, Multispecies, and Oaks. Taxon 25(2/3), 233-239. (DOI 10.2307/1219444)

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