Purdue News
Purdue News
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July 2001 Sex lives of wild fish: genetic techniques provide
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By using genetic fingerprinting techniques such as those used to identify criminals, Andrew DeWoody, assistant professor of forestry and natural resources at Purdue University, and his colleagues, have been able to glean new knowledge about an underwater world of peculiar liaisons.
The findings were published in three scientific papers, including the Proceedings of the National Academy of Science.
Most freshwater fish familiar to sport fishermen reproduce by building nests and laying eggs in the spring. But unlike birds and reptiles, in many freshwater fish species it is the male that builds and tends the nest.
"They try to build an attractive nest to entice females to come and spawn with them," DeWoody says.
Nearly all freshwater fish are external fertilizers, which means that while the female deposits some or all of her eggs in a nest, the male swims over the nest and fertilizes the eggs. The female leaves – often to find another male to spawn with – while the guardian male waits, fanning his tail to aerate the eggs, protecting the nest from predators and hoping to entice another female to add more eggs to the nest.
There's also a problem with other males. "Occasionally a second male will join the spawning pair and attempt to 'steal' fertilizations from the primary male," DeWoody says.
It's a long, lonely vigil hovering over the nest, and the males can't leave for any reason, even to forage for food. "As soon as they leave the nest, minnows or some other fish would come in and destroy the nest by eating the eggs," DeWoody says.
Instead, the males survive by eating a few of the eggs themselves. DeWoody and his colleagues wondered if the males cannibalize just the eggs fertilized by other males, or if they are indiscriminate?
For the study published in the Proceedings of the National Academy of Sciences, DeWoody and the others captured male darters and sunfish to extract undigested eggs from their stomachs. They then used DNA fingerprinting techniques to compare the DNA of the adults with that of the embryos.
They found that the males were unable to distinguish between eggs that were their kin and those that weren't.
"These findings have implications not only for fish ecologists, but also other areas of biology," DeWoody says. "The question of how well animals are able to recognize their kin is a question that many biologists are asking."
But cannibalism isn't the most bizarre part of the spring spawning season. Even for fish, it turns out that it's not always a father-knows-best kind of world. There are other males on the prowl, and these males use deceptive tactics to ensure that they, too, have small fry.
DeWoody and his colleagues also have studied sunfish and found that as few as 85 percent of the fish were nest-builders, which scientists called bourgeois males. The rest, the researchers found, used their unusual sexual development to trick the bourgeois males and reproduce.
There are two types of non-bourgeois males, which scientists call sneakers and satellites.
Sneakers are adult males disguised as immature males. Besides their smaller size and immature appearance, the sneaker males have another difference: dissections show that despite their size, sneakers' testes are three times as large as those of a bourgeois male. "They're not much more than a swimming sack of sperm," DeWoody says.
As their name implies, sneakers approach a nest guarded by a bourgeois male and, when the moment is right, darts over the nest.
"With no cooperation from the female, as the two fish are spawning, this other male zooms in and releases his gametes," DeWoody says.
The second type of parasite male is even more deceptive. The satellite males lack the colorful pigmentation of bourgeois male sunfish, and they are smaller than a typical male. They look almost exactly like a female sunfish. The satellite sunfish approaches the nest as if it, too, wants to spawn with the bourgeois male, but instead of releasing eggs it releases sperm.
The question for fish ecologists has always been, how successful are these alternate fertilization strategies? Not very, the researchers discovered.
DeWoody and his colleagues examined the genetics of the nests to determine how successful these alternate approaches were, and found that the parasitic males only sired 1.3 percent of the embryos.
The genetic data also showed that each of the nests had been spawned by an average of more than seven females.
These results were published in the scientific journal Molecular Ecology.
But not all freshwater fish are so promiscuous. DeWoody and his colleagues found that the most popular sport fish in the United States, the largemouth bass, is unusual for two reasons: Bass are largely monogamous (at least for one season), and both parents are responsible for guarding the nest.
By using the same gene marker techniques used in the other studies, they determined that only 12 percent of the largemouth bass nests contained any eggs fertilized by another male.
"Cuckoldry by males was rare," the researchers noted in a paper published in the December edition of the Proceedings of the Royal Society of London. "The genetic data also revealed that some nests contain juveniles that were not the progeny of the guardian females, a finding that can be thought of as low-level cuckoldry."
"For the most part, you can say that largemouth bass are monogamous," DeWoody says. "This appears to be the first documentation of monogamy and biparental care in externally fertilizing vertebrates."
DeWoody says such advances in the ecology of fish and wildlife is only possible because of advances in genetic techniques. "Genetics in fish and wildlife is always 10 years behind what it is in humans, he says. "But we would not have been able to gather this information without these techniques."
Co-authors on the Proceedings of the National Academy of Science paper were John C. Avise of the University of Georgia, Dean Fletcher of the Savannah River Ecology Laboratory in Aiken, S.C., and David Wilkins of the South Carolina Aquarium.
Source: Andrew DeWoody, (765) 496-6109; dewoody@fnr.purdue.edu
Writer: Steve Tally, (765) 494-9809; tally@aes.purdue.edu
Purdue Ag Communications: (765) 494-2722; Beth Forbes, Ag News Coordinator, bforbes@aes.purdue.edu; https://persephone.agcom.purdue.edu/AgCom/news/
NOTE TO JOURNALISTS: Copies of the PNAS journal article referred to in this release are available from the National Academy of Science at (212) 334-2138.
PHOTO CAPTION: Male freshwater fish, such as these sunfish, guard nests (the light-colored circles) of their eggs against predators and other males. New genetic information by Purdue Assistant Professor Andrew DeWoody reveals that the fish are willing to eat some of their own eggs in order to survive while guarding the nest. (Purdue Agricultural Communications Service Photo donated by Dean Fletcher, Savannah River Ecology Laboratory.)
A publication-quality photograph is available at the News Service Web site and at the ftp site. Photo ID: DeWoody.nests
ABSTRACT
from the Proceedings of the National Academy of Science
Genetic documentation of filial cannibalism in nature
J. Andrew DeWoody, Dean E. Fletcher, S. David Wilkins,
and John C. Avise
Cannibalism is widespread in natural populations of fishes, where the stomachs of adults frequently contain conspecific juveniles. Furthermore, field observations suggest that guardian males routinely eat offspring from their own nests. However, recent genetic paternity analyses have shown that fish nests often contain embryos not sired by the nest-tending male (because of cuckoldry events, egg thievery, or nest piracy). Such findings, coupled with the fact that several fish species have known capabilities for distinguishing kin from nonkin, raise the possibility that cannibalism by guardian males is directed primarily or exclusively toward unrelated embryos in their nests. Here, we test this hypothesis by collecting freshly cannibalized embryos from the stomachs of several nest-tending darter and sunfish males in nature and determining their genetic parentage by using polymorsphic microsatellite markers. Our molecular results clearly indicate that guardian males do indeed consume their own genetic offspring, even when unrelated (foster) embryos are present within the nest. These data provide genetic documentation of filial cannibalism in nature. Furthermore, they suggest that the phenomenon may result, at least in part, from an inability of guardians to differentiate between kin and nonkin within their own nests.
ABSTRACT from Molecular Ecology
The genetic mating system of spotted sunfish (Lepomis punctatus): mate numbers and the influence of male reproductive parasites
J.A. DeWoody, D.E. Fletcher, N. Mackiewicz, S.D. Wilkens
and J.C. Avise
In nest-building fish species, mature males often exhibit one of two alternative reproductive behaviors. Bourgeois males build nests, court females, and guard their eggs. Parasitic cuckolders attempt to steal fertilizations from bourgeois males and do not invest in parental care. Previous evidence from the bluegill sunfish (Lepomis macrochirus) suggests that adult males are morphologically specialized for these two tactics. Here we used micro satellite markers to determine genetic parentage in a natural population of the spotted sunfish (L. punctatus) that also displayed both bourgeois and parasitic male morphs. As gauged by relative investments in gonadal v. somatic tissues, between 5 and 15 percent of the mature adult males were parasites. Multi-locus genotypes were generated for more than 1400 embryos in 30 nests, their nest-guardian males, and for other adults in the population. Progeny in approximately 57 percent of the nests were sired exclusively by the guardian male, but the remaining nests contained embryos resulting from cuckoldry as well. Overall, the frequency of offspring resulting from stolen fertilizations was only 1.3 percent, indicating that the great majority of paternity is by bourgeois nesting males. With regard to maternity, 87 percent of the nests had at least three dams, and computer simulations estimate that about 7.2 dams spawned per nest.
ABSTRACT
from the Proceedings of the Royal Society of London
Genetic monogamy and biparental care in an externally fertilizing fish, the largemouth bass (Micropterus salmoides)
J. Andrew DeWoody, Dean E. Fletcher, S. David Wilkins,
William S. Nelson and John C. Avise
Breeding, male North American sunfish (Centrarchidae) are often brightly colored and promiscuous. however, the largemouth bass (Micropterus salmoides) is sexually monomorphic in appearance and socially monogamous. Unlike some other nest-tending centrachids in the genus Lepomis, largemouth bass have also been reported to provide biparental care to eggs and fry. Here we use microsatellite markers in order to test whether social monogamy predicts genetic monogamy in the largemouth bass. Offspring were collected from 26 nests each usually guarded by a pair of adults, many of which were also captured. Twenty-three of these progeny cohorts (88 percent) proved to be composed almost exclusively of full-sibs and revealed that some nests contain juveniles that were not the progeny of the guardian female, a finding that can be thought of as low-level "female cuckoldry." Overall, however, the data provide what may be the first genetic documentation of near-monogamy and biparental care in a vertebrate with external fertilization.
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