In 1871 the book “The descent of man and selection in relation to sex” by Charles Darwin was published. In that book, it was presented one of the more original and influential scientific contributions by the great man, that of sexual selection. While evolution and even natural selection were not new ideas by Darwin, sexual selection was. Sexual selection explains how males compete for mating females to pass on their genes to future generations, with evolution favoring any treat that could help a male to secure progeny. Sexual selection is sometimes considered part of natural selection, with the difference that the aim is to compete with other males of the same species, instead of gaining survival fitness in competition with individuals of different species found in a given habitat.
In many cases, sexual selection involves the development of sexually attractive traits that may handicap male’s survival fitness, directing evolution in an apparent opposite direction than natural selection would. The examples are numerous; in relation to fish, consider the long bright tail extension of a Xiphophorus swordtail male (a poeciliid), which creates the appearance of a bigger male and thus helps in attracting females (Rosenthal & Evans, 1998), but at the same time possibly attracts predators, or if it is too long, makes swimming difficult. Males which possess the preferred trait (e.g. the long swordtail of the Xiphophorus), will reinforce it by producing more fry than males which do not have such trait, developing with every generation a more attractive (and exaggerated) trait, which may ultimately pose a cost to survival (an overly long sword that may impede fast swimming) to a point that the trait is stabilized at a maximum allowed by natural selection. The development of a trait that attracts females, but at the same time impedes fitness, which the male is still able to surmount, is known as the handicap principle.
Of course not always an attractive trait will reduce fitness (at least significantly) to a male. Perceived attractive traits in males are reinforced in every generation by the females’ selection of males that have them, resulting in even more beautiful males, every time more different from females. This is what causes sexual dimorphism, with males so different from females that sometimes they may seem to be different species. Males, normally being the limited sex, develop these traits that make them more attractive to females.
In some cases, sexual selection directs evolution to create much larger, stronger males, who can compete with other males for the favor of females, leading males to be much bigger than their sexual counterparts; this is known as intra-sexual selection. In many cichlid species, males are larger than females. We have one extreme example in the Lake Tanganyika cichlid ‘Lamprologus’ callipterus, whose males are up to 60 times heavier than females. In this harem brooding species, only the larger and strongest males are capable to sire broods, which require them to establish and successfully defend a shell garden, often stealing shells from neighboring males (Konings, 2013).
Not always it is size or color that attracts females to a particular male, but the territory they establish and hold.
In an experiment done by Mindy Nelson (1995) where she studied females’ preference for males of the species Oreochromis mossambicus, an African cichlid whose males build nests in sand-muddy areas to which they attract females to spawn, she found that females would select for larger males, but given males of the same size, females would chose the male that had built the largest nest.
Enantiopus malanogenys is an open sandy substrate dweller which occurs throughout Lake Tanganyika and outside reproduction lives in large schools, with most individuals of a single school remaining together throughout their lives. At spawning time, males chose a sandy area among rocks in shallow water and establish a territory for breeding, which they meticulously prepare for that end. The territory consists of a flat saucer shaped circle of around 50 cm, delimited with a sand rim. In the center of the territory the male digs a small shallow pit with a diameter of about 15 cm where spawning takes place. The spawning dishes are meticulously cleaned of small pebbles which are larger than the prevailing sand grains, so that the female cannot mistake a tiny pebble for an egg when she collects them in the mouth after spawning (Konings, 2011).
Once the territory is ready, males circle it and defend it from other males by displaying to them aggressively with all fins erected. When females approach, the male adopts a humble pose closing its fins and laying on its side. If the female accepts the male, she will enter his territory and the male, getting excited, circle her with his fins erects, guiding her to the spawning area where spawning occurs. The female then deposits her eggs in several runs, which get fertilized by the male before she collects them all in the mouth and leaves.
In Lake Malawi, Stauffer et al. (2005) demonstrated that males of Lethrinops parvidens that build higher bowers would get more females to visit them and fertilized more eggs than those males that build lower bowers.
Preventing hybridization and driving speciation
Sexual selection is a force that prevents hybridization between similar species and at the same time drives speciation. For a cichlid female, which is normally the limiting sex (which selects partners) it is very expensive to make a mistake about the male they choose, since they have to invest a large amount of resources into the developing and care of eggs and bringing up of their fry, and hence there are natural mechanisms that allow them to select the proper male.
Apistogramma dwarf cichlids are in most (if not all) cases polygamous harem forming species. Males defend territories where several females are hosted for breeding purposes, a type of polygamy more specifically known as polygyny. Females in Apistogramma depend significantly on male coloration to select mates (Römer et al., 2005), discriminating males that do not have the right coloration. Hence the importance of the evolutionary development of a correct, bright, and easily discernible coloration in males, which at the same time may significantly differ from that of females. Unlike African polygynous mouth-brooding species, where females are only modestly colored and difficult to tell apart from similar species, Apistogramma females are brightly colored, normally bright yellow, and strikingly marked with distinctive patterns of black on the flanks and fins. This may be due to their need to hold smaller territories inside the male territory and offer prolonged care of their fry, interacting in the meantime with neighboring females’ territories (Barlow, 2002).
In Lake Malawi Knight & Turner (2004) demonstrated that color differences among allopatric (geographically separated) populations of the rocky reef dwelling mbuna Metriaclima zebra cause females to discriminate males. The researchers found that just in 20% of the cases females would not select males of their own geographic race, with males with somewhat different color pattern rejected.
A similar experiment (Egger et al., 2008) was conducted with different color morphs of Lake Tanganyika Tropheus species, a social cichlid inhabiting the upper ten meters of the rocky biotope where they gregariously feed on algal strands combed out of the periphyton. Testing female preferences for males of different geographical races, the researchers found that in almost cases (13 versus 1) females would court males of the same color morph.
In Lake Victoria in Africa, females of two sympatric (living together) species of haplochromine cichlids: Pundamilia nyererei and P. pundamilia, discern between males of these two morphologically very similar species on the basis of coloration (Selz et al., 2014). Males of P. nyererei are red and those of P. pundamilia blue. In this particular example the specific color of the male, which should be highly visible, helps males not only to get a partner, but also prevents the two species to hybridize and dilute into one hybrid species. Females on the other hand, being those that select for males, do not need any special coloration and normally have just drab colors, and in many cases, are almost impossible to tell apart. The correct female selection is the driving force behind speciation in these two species.
However, the very same mechanism that prevents hybridization, which is females’ selection of males based on their nuptial coloration, is now facilitating it by the increasing turbidity of water in some areas and the consequent failure of females to clearly recognize their own males. In the two previously mentioned species: Pundamilia nyererei and P. pundamilia, a higher hybridization rate has been observed in areas of decreased water transparency (Maan et al., 2010). This effect has been observed in other polygynous species in Lake Victoria.
Nests built by males of different species may as well serve as a species delimitation instrument. In Lake Malawi, males of several species build castle like sand structures commonly referred as bowers for the spawning to take place. McKaye et al. (1993) compared bower shape and genetic distance between closely related species of Tramitochromis obtaining results that suggest that different shaped bowers help females to identify their kind and prevent them from hybridizing.
Although in polygynous species females are regularly those that discriminate between males of its own kin and others, this is not always a one way street. When females are discernible, males would also be able to tell the difference and chase those females of a different species away. In an experiment with two mbuna cichlid species, Holzberg (1978) found that males of Metriaclima zebra and M. callainos would come out and court females of its kin and chase away those that weren’t.
When male and females look alike
In all of the cichlid species covered so far males and females show significant sexual dimorphism, not just in size, but more importantly, in traits like color and morphology. This is a typical situation in polygamous cichlids. There are however many cichlid species whose gender are very difficult to tell, since they do not show other sexual dimorphism than in some cases differences in size or other minor traits. In most of these cases these are monogamous, substrate brooding species. How do then males and females can differentiate each other?
Even when males of monogamous cichlids grow more than females, it is hard to assess sexes just because of size, since fish grow all through their lives. Certainly, one can be reasonably sure a fish is a male when its size is more than the maximum any given female could reach, but that is not enough, since cichlids are sexually mature at a much earlier stage of their lives and it is easy to find mature males which are smaller than mature females. Size alone is not a reliable determiner for gender; cichlids should look for other traits.
In experiments made on three very similar Middle American cichlid species of the genus Amphilophus: A. citrinellus (the midas cichlid), A. labiatus (the red devil) and A. zaliosus (the arrow cichlid), which live sympatrically in some areas of the San Juan River drainage in Nicaragua, but not in others, some clues where found. These three species are almost undistinguishable visually and between the sexes. Jeff Baylis (1976) observed that naturally sympatric A. citrinellus and A. zaliosus interbred and produce viable hybrid offspring in the laboratory, when given no mating choice except a mate of the opposite species, but they would not interbreed when given a choice. Baylis concluded that a complex web of communication between them prevented them from interbreeding.
Jennifer Holder (1991) carried out more experiments in A. citrinellus and A. labiatus housing them in adjacent quarters where they could have both visual and/or chemical contact, she observed if under different conditions the fish would exhibit courtship display. She discovered that both visual and chemical signals are necessary for the correct identification of the species. Species recognition on those cichlids, unlike in many other animal species, is based on several cues.
If our current knowledge of how cichlids determine their own species is scarce, that of how species without sexual dimorphism determine the gender of a potential partner is even scarcer.
Males of some species develop a hump produced by water filling the fatty tissue in the forehead; this hump appears in males around courting time and disappears around spawning time. I have personally observed the appearance and disappearance of such hump on males of Herichtys tamasopoensis in the Gallinas River, a Panuco River affluent in Mexico, in such periods. This hump appears in many monogamous or polygamous cichlids. The hump is quite likely one of the visual clues females use to determine males.
Other than visual cues, sound signals may also be used as sex determiner; Barlow (2002:143) describes how Archocentrus centrarchus males, a Central American cichlid, produce low-pitched grunting sounds with higher frequency when they see a female, reducing the grunts if the female shows courting behavior.
For pairs of cichlids to remain bonded, it is plausible to accept that there is an individual constant recognition of each other, as approaching the wrong individual by a pair member could turn out to be very costly, or fatal. This recognition is also important so the pair is not vigorously fighting neighboring pairs with which territory boundaries have been already set, which would be a waste of energy. Beyond this, it is widely accepted by cichlid keepers that individual cichlids recognize their keeper and other people. Think on how many times the keeper is inside his fishroom with all cichlids either behaving causally or asking for food, only to immediately flee for cover when an unknown visitor to which the keeper wants to show off the fish appears? Clearly, visual recognition plays a big paper in sex or species recognition alike.
In monogamous cichlids, both sexes tend to mate with the larger, more aggressive partner they can find. A female wants a large male that is able to defend the territory and the fry from potential predators, and a male wants a big female to produce many eggs - since egg size is constant for a species regardless of the size of the female (Coleman, 1998). One more thing is important for a male: that the potential partner female is ready to spawn. It has been observed that a male can probably assess the readiness of the female in at least in two ways: one is to look at the female’s rounded girth full of eggs; the second is to look at her genital papillae (Schwanck, 1987; Barlow, 1992), which is blunt when a female is ready to spawn. A male will prefer a smaller female ready to spawn than a larger female which is not (Nuttal et al., 1993). For a female this is not so important since courting males are always ready to spawn, since time and energy necessary to produce sperm is much less than what it takes a female to produce the eggs.
In a group of one male and two females of Vieja zonata, a Middle American cichlid, I observed that between the two females, the male would always chose the largest as spawning mate, but when a spawning with her went wrong, he demanded the female to spawn again immediately, which given the time it takes to produce eggs wasn’t possible. The male then switched to court the smaller female, which was ready to spawn, and between the two of them chased away the larger female from the territory. Of course this is just one observation, but I predict that more than one cichlid keeper has replicated it.
During courtship in monogamous cichlids pairs, the strength of the potential mate is often tested, among other ways, by locking their jaws and twist, this is made to make sure the potential mate is fit and strong enough. Sometimes, these testing matches end in a real fight and the weaker individual, normally the female, has to flee.
One interesting experiment by George Barlow in this regard is described in his book (Barlow, 2002:150). Having aquariums where a female had access to two individual males separated each one from the female by a divider, where they could see each other and interact through the barrier but not get together. The males were equally sized but had different aggression levels. They observed that the females would always get close and court the most aggressive of the males. It all seemed to go good for pair formation, but after the screen between the two was removed, in about half of the occasions they would not pair up, with the male attacking the female, which had to be rescued. Some aggressive males had rejected the females based on their low aggressiveness. If the rejected females were put together with the less aggressive males, in many cases they would pair up. It was concluded from the experiment that it is not always the female in a monogamous pair that makes the mate selection. It seems that a higher level of aggressiveness was requested from the female by the aggressive male!
There is a lot to be learned about mating mechanism in cichlids, and many more studies are necessary to clarify the behavioral and physiological aspects that lead to a successful match. It is quite a fascinating topic! As in other occasions, for a more insightful treatment of this topic I heartily recommend the wonderful book by George Barlow "The Cichlid Fishes (Nature's Grand Experiment in Evolution)", chapters 7 (Beauty is only fin deep) and 8 (Mating gets personal).
- Barlow, George W.. 2002. "The Cichlid Fishes (Nature's Grand Experiment in Evolution)". Perseus Publishing. pp. 352 pp. ISBN: 9780738203768 (crc03927) (riassunto)
- Barlow, George W.. 1992. "Mechanisms of mate choice in monogamy". Behavioral mechanisms in evolutionary perspective. Madrid Instituto Juan March de Estudios e Investigaciones. pp. 26-29 (crc09374)
- Baylis, Jeffrey R. 1976. "A quantitative study of long term courtship: I.Ethological isolation between sympatric populations of the midas cichlid, C. citrinellum and the arrow cichlid, C. zaliosum". Behaviour. v. 59,(n. 1), pp. 59-69. DOI: 10.1163/156853976X00460 (crc09370) (riassunto)
- Coleman, Ron. 1998. "Cichlids and Science: Enigmatic Eggs". Cichlid News Magazine (crc00552)
- Egger, Bernd & B. Obermüller, E. Eigner, C. Sturmbauer, K.M. Sefc. 2008. "Assortative mating preferences between colour morphs of the endemic Lake Tanganyika cichlid genus Tropheus". Hydrobiologia. v. 615(n. 1), pp. 37-48. DOI: 10.1007/s10750-008-9564-0 (crc03670) (riassunto)
- Holder, Jennifer L. 1991. "The mechanisms of mate choice in the Midas cichlid Cichlasoma citrinellum". Unpublished Ph.D. dissertation, University of California, Berkeley (crc09372)
- Holzberg, S. 1978. "A field and laboratory study of the behaviour and ecology of Pseudotropheus zebra (Boulenger), an endemic cichlid of Lake Malawi (Pisces; Cichlidae)". Journal of Zoological Systematics and Evolutionary Research. v. 16(n. 3), pp. 171-187. DOI: 10.1111/j.1439-0469.1978.tb00929.x (crc04855) (riassunto)
- Knight, Mairi E & Turner, G.F. 2004. "Laboratory mating trials indicate incipient speciation by sexual selection among populations of the cichlid fish Pseudotropheus zebra from Lake Malawi". Proceedings of the Zoological Society of London. 271: 675-680 (crc02342) (riassunto)
- Konings, Ad. 2013. "Species profile: exLamprologus callipterus (Boulenger, 1906)". The Cichlid Room Companion. URL consultato in data 19-feb-2021, da: https://cichlidae.com/species.php?id=58 (crc10245) (riassunto)
- Konings, Ad. 2011. "Species profile: Enantiopus melanogenys (Boulenger, 1898)". The Cichlid Room Companion. URL consultato in data 19-feb-2021, da: https://cichlidae.com/species.php?id=41 (crc10235) (riassunto)
- Maan, Martine E & O. Seehausen, JJM. Van Alphen. 2010. "Female mating preferences and male coloration covary with water transparency in a Lake Victoria cichlid fish". Biological Journal of the Linnean Society. v. 99(2): pp. 398-406 (crc02462) (riassunto)
- McKaye, Kenneth R. & J.H. Howard, J.R. Stauffer, Jr., R.P. Morgan, F. Shonhiwa. 1993. "Sexual Selection and Genetic Relationships of a Sibling Species Complex of Bower Building Cichlids in Lake Malawi, Africa". Japanese Journal of Ichthyology. v. 40(n. 1), pp. 15-21 (crc05336) (riassunto)
- Nelson, C. Mindy. 1995. "Male size, spawning pit size, and female mate choice in a lekking cichlid fish". Animal Behaviour. v. 50(n. 6), pp. 1587-1599 (crc09369) (riassunto)
- Nuttal, B. D. & M.H.A. Keenleyside. 1993. "Mate Choice by the Male Convict Cichlid Cichlasoma nigrofasciatum: Pisces, Cichlidae". Ethology. v.95(3), pp. 247-256. DOI: 10.1111/j.1439-0310.1993.tb004 (crc01819) (riassunto)
- Römer, Uwe & W. Beisenherz. 2005. "Intra- and interspecific mate choice of female Apistogramma cacatuoides (Teleostei: Cichlidae)". Ichthyological Explorations of Freshwaters. v. 16(n. 4), pp. 339-345 (crc02500) (riassunto)
- Schwanck, E. 1987. "Female mate choice in Tilapia mariae". Unpublished Ph.D. dissertation, University of Stockholm (crc09373)
- Selz, Oliver M. & M.E.R. Pierotti, M.E. Maan, C. Schmid, O. Seehausen. 2014. "Female preference for male color is necessary and sufficient for assortative mating in 2 cichlid sister species". Behavioral Ecology. (n. epub), pp. 1-15. DOI: 10.1093/beheco/aru024 (crc06279) (riassunto)
- Stauffer, Jay Richard Jr. & K.A. Kellogg, K.R. McKaye. 2005. "Experimental evidence of female choice in Lake Malawi cichlids". Copeia. v. 2005(n. 3), pp. 657-660. DOI: 10.1643/CE-04-326R (crc02431) (riassunto)
© Copyright 2021 Juan Miguel Artigas Azas, all rights reserved
Artigas Azas, Juan Miguel. (febbraio 19, 2021). "Mate selection in cichlids". Cichlid Room Companion. URL consultato in data aprile 13, 2021, da: https://cichlidae.com/section.php?id=314&lang=it.