Molecular ecology
Terrestrial zoologists are fortunate in that they can observe the behavior of study organisms with relative ease. Yet when molecular assays are applied, it becomes apparent that these studies can miss important facets of life history, especially in breeding biology. Perhaps terrestrial zoologists are complacent, or sleep too much. Regardless of the explanation, these problems are compounded in the aquatic medium, as observations of natural behavior are more difficult to make and are often limited in duration.
In the period when allozyme studies dominated population genetics, practitioners had to carry dry ice or cumbersome vats of liquid nitrogen to their field locations to collect and preserve fresh tissue. Many older ichthyologists remember this era of difficult methods, and they shunned collections of genetic materials as part of their field activities.
These days the collection of material for genetic analysis could hardly be easier. The PCR process (see above) requires only small quantities of intact DNA. No freezing or refrigeration is necessary to preserve specimens, and a tiny amount of tissue (less than 0.5 g) is suffi cient for DNA analyses. The field collector only has to prevent DNA degradation by bacteria, fungi, or harsh environmental conditions. This can be accomplished by storing tissue in isopropyl alcohol (>50% preferred), ethanol (>70% preferred), or a saturated salt (NaCl) solution. In a pinch, ichthyologists have used distilled spirits, which are usually available at even the most remote field sites.
Today’s collecting kit for fish genetics is no larger than a lunch box, and contains no toxic or corrosive materials that might complicate air travel. Any field expedition can include one. Even if the field researchers are not directly interested in genetic analysis, they can support tissue collections that advance many areas of ichthyology. The University of Kansas Natural History Museum maintains one of the oldest and largest fish tissue collections (http://nhm. ku.edu/fishes/).
Molecular genetics in general, and microsatellite markers in particular, have launched a renaissance in the field of reproductive biology. Previous conclusions about breeding systems that have accrued over many decades, often requiring labor-intensive observations, can now be efficiently tested with individual-specific genetic markers. Questions about monogamy (couples mating only with each other), multiple paternity and maternity in egg clutches, egg thievery, and cuckoldry can be resolved. Microsatellites also allow genetic reconstructions of family pedigrees with a high degree of certainty. These genetic tools have highlighted the distinction between social mating systems, as defined by behavior, and genetic mating systems, as defined by relationships in a DNA-based pedigree. For example, social monogamy in nesting fishes is often coupled with genetic cuckoldry, indicating that fi delity among mates is less widespread than previously assumed. Multiple paternity or maternity in a clutch of eggs can be readily detected based on the number of alleles observed
at microsatellite loci. The methodology is straightforward in diploid organisms: survey individuals in a brood (eggs or offspring) with microsatellite markers. At eachautosomal (not sex-linked) locus, the maximum number of alleles in the offspring of a monogamous brood is four (two from the mother, two from the father). If five or six alleles are detected, at least three parents (usually including two fathers) are contributing, if seven or eight alleles are detected then at least four parents are contributing. Usually these assays are conducted with three or more microsatellite loci to attain reliable estimates of the number of parents.
To accurately reconstruct family relationships and corresponding breeding systems, it is preferable to genetically survey all candidate parents for a brood of offspring. While this may be achievable in large mammals (including humans), it is seldom a practical goal with fishes, and is impossible in pelagic-spawning marine fishes. In these cases, statistical methods can be employed, particularly maximum likelihood, to estimate parental assignments (Bernatchez & Duchesne 2000).
The level of multiple paternity/maternity in marine fishes with pelagic larval dispersal is unknown. In fishes that spawn in aggregations (including many pelagic fishes), monogamy could be uncommon. On the other hand, fishes that breed as stable pairs (including many coral reef fishes) could have a high degree of monogamy. For these cases, researchers have long wondered whether siblings could stay together during the pelagic larval phase, and recruit to the subadult habitat as a group of related individuals (Shapiro 1983). This runs counter to the long-held view that marine fish larvae are highly dispersive. Indeed the first genetic test of kinship in young-ofyear reef fishes, based on three allozyme loci, found no evidence of related individuals in the Red Sea serranid Anthias squamipinnis (Avise & Shapiro 1986), and the same conclusion was forwarded recently for the clownfish Amphiprion percula, based on seven microsatellite loci (Buston et al. 2007).
However, several recent lines of evidence indicate that fish larvae have advanced swimming and navigational skills (Leis & Carson-Ewart 2000b) and some can recruit back to their region of origin (Jones et al. 2005). These observations resurrect the possibility that kin groups (siblings) can remain together in the pelagic phase and settle out on the same reef habitat. Three recent studies provide evidence for this behavior. Planes et al. (2002) used allozymes to survey juveniles of the Unicornfish (Naso unicornis) recruiting to Pacific reefs and observed high relatedness within these groups. Pujolar et al. (2006) found high relatedness within some cohorts of the catadromous eel (Anguilla anguilla) recruiting to European streams. These findings are remarkable given that European eel larvae may spend more than a year in the pelagic zone prior to transforming into juveniles. Selkoe et al. (2006) conducted microsatellite surveys to assess recruits of the Kelp Bass (Paralabrax clathratus) on the West coast of North America. The application of kinship tests, not available to previous studies, revealed siblings and half-siblings (sharing one parent) in seven out of 40 samples. Hence evidence of kinship among recruits of marine fishes is increasing. However, these studies indicate that the phenomenon is not consistently observed in all groups of recruits, even within a single species and region.
Among the egg-laying (oviparous) fishes, nest guarding (usually by males) occurs in marine and anadromous fishes but is most common in freshwater species. Here the genetic surveys support previous suggestions that monogamy is frequently subverted by sneaker males (those that do not maintain a nest but deposit sperm into other nests) and other forms of cuckoldry, nest takeovers, and egg thievery. Furthermore, genetic studies have begun to reveal the success rate of these alternative breeding strategies. In a review of the genetic literature on the mating systems of fishes, DeWoody and Avise (2001) reported that when males guard the nest, on average they retain about 70–95% of paternal contributions. The remainder can be either from males that maintain nearby nests, or sneaker males. In this review of 10 species and 177 nests, one-third of nests showed evidence of cuckoldry, and no species was without some level of multiple paternity within nests.
In addition to multiple paternity in male-guarded nests, egg contributions from multiple females are common. In those genetic surveys, microsatellite surveys were augmented with maternally inherited mtDNA, whereby the number of haplotypes indicates a minimum number of mothers. Based on a summary of 10 species, DeWoody and Avise (2001) reported a range of one to 10 mothers pernest, with an average of 3.1 females/nest. In the same survey, the authors reported that eggs from a single female are routinely found in multiple nests. In nesting fishes, cuckoldry works both ways but is rarer in females (Avise et al. 2002).
Egg thievery is a puzzling phenomenon wherein nesting males steal clumps of fertilized eggs from other nests – eggs that have no genetic contribution from their new guardian. In a survey of 24 nests in the 15 spine sticklebacks (Spinachia spinachia), four had eggs that were probably stolen, as indicated by no maternal or paternal affiliation with nest mates (Jones et al. 1998). Why would a male deliberately guard and hatch eggs that are not his own? The most accepted explanation is that stolen eggs “prime” the nest for subsequent egg laying. Neophyte males may pose as successful breeders and guardians, thereby increasing their attractiveness to discriminating females.
Internal fertilization guarantees that the caretaker is the biological mother in all cases. However, rates of multiple paternity are variable across the (primarily freshwater) fishes that bear live young. Chesser et al. (1984) used allozymes to survey broods of the Mosquitofish (Gambusia affi - inis), concluding that 56% of females contained embryos from multiple males. However, a re-examination of this species with microsatellites revealed that the multiple paternity rate is near 100% (Zane et al. 1999). The available evidence indicates that multiple paternity is common and widespread in the live-bearing fishes, as originally predicted by Chesser et al. (1984).
All elasmobranchs have internal fertilization, and most give birth to live young, although a minority, including skates (Rajiformes), horn sharks (Heterodontiformes), and Chimaeras (Chimaeriformes), lay egg sacks. Regardless of the oviparous or viviparous pathway, internal fertilization again guarantees that the female is the biological mother, and also seems to promote multiple paternity. Daly-Engel et al. (2006) used microsatellite data to detect multiple paternity in two out of three surveyed members of genus Carcharhinus (requiem sharks), indicating that the phenomenon may be widespread in elasmobranchs. Microsatellite surveys demonstrated that about 40% of Sandbar Shark (Carcharhinus plumbeus) litters in Hawaii are multiply sired (Daly-Engel et al. 2007), compared to 86% of Lemon Shark (Negaprion brevirostris) litters in the Bahamas (Feldheim et al. 2004), and about 19% of Bonnethead (Sphyrna tiburo) litters in the Gulf of Mexico (Chapman et al. 2004). Hence the limited data indicate that multiple paternity is common but highly variable in elasmobranchs.
Fishes in the family Cichlidae have independently evolved mouth brooding in several genera, wherein fry are retained (primarily in the mother’s mouth) after hatching (Goodwin et al. 1998). The few genetic surveys conducted to date demonstrate both multiple paternity and (more surprisingly) multiple maternity in female mouth-brooders. In the Blue Cichlid (Pseudotropheus zebra), microsatellite markers demonstrate multiple paternity in six of seven broods, and the female brooding the eggs was the mother in all cases (Parker & Kornfield 1996). In the Lake Tanganyika mouthbrooder Tropheus moorii, however, 18 of 19 broods examined with microsatellites had a single father (Egger et al. 2006). In the Lake Malawi mouth-brooder Protomelas spilopterus, microsatellite analyses reveal that four of six mouth-broods in females contained unrelated young at frequencies of 6% to 65% (Kellogg et al. 1998). In other words, females are brooding young from other members of their species. While this may be a simple mix-up between adjacent females, or maladaptive behavior, hypothesized benefits include attraction of mates, increased survivorship of siblings by dilution effect, and kin selection (aiding close relatives).
It is not clear that the mating behavior of mouthbrooders should be different from other egg-laying (oviparous) fishes. However, mouth brooding apparently confers much stronger population genetic structure than other reproductive behaviors, by eliminating the larval stage and reducing juvenile dispersal (see below, Population genetics). Both the mouth-brooding Banggai Cardinalfish (Pterapogon kauderni, one of the few marine mouth-brooders) and the mouth-brooding tilapia (Sarotherodon melanotheron) show strong genetic separations between populations (Pouyaud et al. 1999a; Hoffman et al. 2005).
The remarkable natural history of the family Syngnathidae (pipefishes and seahorses) has elicited much attentionbecause of the “pregnant” (pouch-brooding) males. Just as internal fertilization guarantees that the viviparous female is the mother of offspring, the pouch brooding by male syngnathids assures that cuckoldry is effectively absent. However, microsatellite studies indicate that the rate of monogamy varies from 10% to 100%, as males may carry eggs from a single female or from as many as six females (Jones & Avise 2001). These same studies indicate that females may contribute eggs to more than one male pouch (polyandry).
In most fish species, females make the greater investment in reproduction, and males must compete for the limiting resource, specifically access to egg-laying females. Sexual selection theory maintains that the gender competing for the limited resource will have more pronounced secondary sexual characteristics (such as bright coloration), will be under stronger sexual selection, and will show a tendency towards multiple mating. The sex role reversal of the syngnathids offers a rare mirror image of typical sex roles, and an opportunity to test sexual selection theories (Vincent et al. 1992). In most (but not all) syngnathids, the males’ pouches, rather than the females’ eggs, are the limiting resource. Hence females compete for space in these pouches and, consistent with theory, display characteristics that are usually associated with males:
1 When sexual dimorphism is apparent in syngnathids, it is usually the females that display the conspicuous ornamentation (Dawson 1985).
2 In the few cases where sexual selection (for reproductive success) has been measured in sygnathids, it is higher in females than males (Jones et al. 2001).
3 Although there is considerable variation in sygnathid mating systems, microsatellite surveys show a range from monogamy to polyandry (multiple males mating with a single female), rather than the predominant polygyny (multiple females mating with a single male) observed in nesting fishes (Avise et al. 2002).
The research to date generally confi rms sexual selection theories that were originally formulated in the realm of male sexual selection and polygyny.
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