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Evolutionarily Significant Units Among Cichlid Fishes: the Role of Behavioral Studies

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Evolutionarily Significant Units Among Cichlid Fishes: the Role of Behavioral Studies American Fisheries Society Symposium 17:227-244. 1995 © Copyright by the American Fisheries Society 1995 Evolutionarily Significant Units among Cichlid Fishes: The Role of Behavioral Studies Jay R. Stauffer, Jr. and N. J. Bowers1 School o f Forest Resources, The Pennsylvania Slate University University Park, Pennsylvania 16802, USA K e n n e t h R . M c K a y e Appalachian Environmental Laboratory. University of Maryland Frostburg, Maryland 21532. USA T hom as D . K o c h e r Department of Zoology, University of Sew Hampshire Durham, .Wew Hampshire 01823, USA Abstract.—Cichlid fishes represent an outstanding case of explosive evolution and offer extraordi­ nary opportunities to investigate the evolutionary processes that have led to such diversity. Throughout the world, however, these fishes are threatened by overfishing, introduction of exotics, habitat destruction, and pollution of the environment. Determination of the specific status of local taxonomic units is critical for the development of programs both to conserve and to utilize these fishes for food, tourism, disease control, and scientific investigations. Rapid speciation within these fishes, however, has resulted in a paucity of characters for discriminating among species. Our experiences in Africa and Central America demonstrate that in situ behavioral studies, integrated with morphological and genetic analysis of taxonomic units, are vital to determining the specific status and relationships among evolutionarily significant units (ESUs). The critical element in determining whether a taxon is an ESU is knowledge of its reproductive biology; therefore, it is imperative that we develop a multidisciplinary emphasis in biodiversity studies. The phrase evolutionarily significant unit (ESU) small disjunct population in the Monongahela implies that (1) a heritable difference exists among River system in West Virginia. Maryland, and populations; (2) an important statistical difference Pennsylvania (Stauffer et al. 1995). If this disjunct exists in a group of characters among units: and (3) population were designated as an ESU. then per­ a classification system is being used. From a pure haps a vehicle would be in place to protect this conservation point of view, any such ESU must be unique population of a widely dispersed species. protected. We are not suggesting that the term ESU Minimally, an ESU may be a population that replace our concept of a species or other formally exhibits a distinctive behavior. The importance of recognized taxonomic category but that it be used behavior in distinguishing among fish taxa was pio­ to recognize unique entities that need protection. neered by Trewavas (1983), who used behavioral For example. Waples (1991) suggested that a pop­ characters when delimiting three genera of tilapiine ulation should be considered an ESU if it is repro- fishes. In many cases, behavioral studies are instru­ ductivelv isolated from other conspecific popula­ mental in recognizing novel entities, assigning pop­ tions and if it represents an important component in ulations to taxa (Brooks and McLennan 1991), and the evolutionary trajectory of the species. Evolu­ estimating phylogenetic relationships among taxa tionarily significant units may also be defined geo­ (Wenzel 1992; deQueiroz and Wimberger 1993). graphically. in that they may be a particular com­ Nowhere is the designation and protection of munity or ecosystem that harbors a highly diverse ESUs needed more than in tropical ecosystems. It is fauna or flora or is a site of high endemism. Por­ estimated that as many as half of the extant species tions of a widespread population that has a disjunct inhabit the approximately 6% of the earth covered distribution may be designated as an ESU. For with tropical rain forests (Myers 1988). With re­ example, the longnose sucker Catostomus catosto- spect to fishes, there are 66 families endemic to mus (Forster) is panmictic; however, there exists a tropical freshwaters, whereas only 18 are endemic to temperate freshwaters (Berra 1981); moreover, ‘Present address: Environmental Sciences and Re­ greater than 70% of the described species of fishes sources. Portland State Universitv, Portland. Oregon inhabit the tropics (Moyle and Cech 1988). One of 97207. U SA the most speciose families of freshwater fishes is the STAUFFER ET AL. Cichlidae. thus many of the examples that follow cal separation, ethological isolation, and allochronic will be from this family. mating. The development of many premating bar­ riers are the direct consequence of changes in be­ Species Concepts havioral characters. Several investigators have suggested that specia­ In part, the concept of the ESU involves grouping tion of cichlids may have occurred svmpatrically as individuals or populations into distinct taxa. which, well as allopatricallv (Fryer and lies 1972; McKave in tum. depends on the definition of species or et al. 1990). In svmpatric speciation models, repro­ some lower hierarchical taxon. Subsequent to the ductive isolating mechanisms originate within the evolutionary synthesis (Mavr 1982a: Eldridge 1985) dispersal area of the offspring produced by a single there has been much debate concerning species deme (Hartl and Clark 1989) and premating isola­ concepts (e.g., Simpson 1961: Wilev 1981: Donog- tion develops before populations inhabit distinct hue 1985: Paterson 1985; Templeton 1989: Mayr niches (Bush 1975). Controversy over the mecha­ 1992: van Devender et al. 1992). This debate can be nisms of svmpatric speciation center around the attributed to a certain degree to some biologists question of how reproductive isolation can arise treating species as epiphenomena. whereas others prior to a barrier to gene flow (Mayr 1982b). Koss- regard species as participants in the evolutionary wig (1963) suggests that populations can be isolated process (Mayr and Ashlock 1991). We would agree ecologically without oven geographical barriers, with Mavr (1992) that a nondimensional (nonhis- due to differences in habitat preference in a varied torican concept of the species is the one with which environment. Factors that may contribute to eco­ most biologists are concerned and which is probably logical isolation of populations include competitive the most applicable to conservation and protection isolation (McKave 1980). seasonal isolation (Lowe- programs. We argue, however, that it is difficult to McConnell 1959), mate selection isolation (Trewa- develop an unambiguous species definition given vas et al. 1972: Barlow and Munsev 1976). and the mixture of conspecific populations, incipient runaway sexual selection (Dominev 1984: McKave species, and good species that predominate in allo- 1991: McKave et al. 1993). In addition, intrapopu- patric populations of freshwater fishes, such as the lational variation in the expression of a given geno­ cichlids. Hence, the ESU provides an effective con­ type due to environmental conditions permits the cept upon which to base conservation practices maximum use of a heterogenous habitat (Liem and when dealing with rapidly evolving groups, such as Kaufman 1984; Via and Lande 1985). Within the the cichlids. cichlids, alternative adaptations (polymorphisms) may also have contributed to the extensive adaptive Speciation radiation and sympatric coexistence of closely re­ The concept of speciation involves the origin of a lated forms (West-Eberhard 19S3). unique gene pool. The processes responsible for the Cichlid fishes throughout the tropics and specif­ ecological separation and reproductive isolation of ically in the Great Lakes of Africa are generally populations have long been debated. Intralacustrine recognized as one of the most dramatic examples of allopatric speciation has been widely purported to extensive trophic radiation and explosive specia­ account for the rapid and extensive speciation by tion. Discrimination among species of Cichlidae can cichlid fishes in the African Great Lakes (Fryer be difficult because differences among species may 1959: Fryer and lies 1972: Mayr 1982b). The first be very small and intraspecific variation may be stage in allopatric speciation is geographical segre­ relatively large (Fryer and lies 1972: Ribbink et al. gation of a single population into two or more 1983). The acquisition of reproductive isolation subpopulations. Speciation culminates with the de­ without significant morphological change makes it velopment of reproductive isolating mechanisms difficult to distinguish African haplochromine cich­ that prevent interbreeding even if the geographical lids (Lewis 1982). Attempts to use starch gel elec­ barriers are removed and the populations experi­ trophoresis have been inconclusive for delimiting ence secondary contact (Mayr 1942). Both pre- and species (Komfield 1974. 1978). McKave et al. postmating isolating mechanisms influence repro­ (1982) electrophoreticallv examined three color ductive isolation among heterospecific populations. morphs of Peirotilapia triilentiger Trewavas (a cichlid Postmating isolating mechanisms include gametic endemic to Lake Malawi) that could not be distin­ mortality, zygotic mortality, hybrid inviability, and guished morphometricallv. They found no fixed al­ hybrid sterility; premating isolating mechanisms in­ leles at any of the 25 loci studied, although allele clude incompatible reproductive anatomy, ecologi­ frequencies were heterogeneous among taxa. sug- BEHAVIORAL STUDIES OF CICHLID FISHES 229 jesting that the color morphs represented isolated Sexual Selection gene pools
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