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SIBLING SPECIES, ADVERTISEMENT CALLS, and REPRODUCTIVE ISOLATION in FROGS of the Leptodactylus Pentadactylus SPECIES CLUSTER (AMPHIBIA, LEPTODACTYLIDAE)

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SIBLING SPECIES, ADVERTISEMENT CALLS, and REPRODUCTIVE ISOLATION in FROGS of the Leptodactylus Pentadactylus SPECIES CLUSTER (AMPHIBIA, LEPTODACTYLIDAE) Herpetologia Petropolitana, Ananjeva N. and Tsinenko O. (eds.), pp. 35 – 39 35 SIBLING SPECIES, ADVERTISEMENT CALLS, AND REPRODUCTIVE ISOLATION IN FROGS OF THE Leptodactylus pentadactylus SPECIES CLUSTER (AMPHIBIA, LEPTODACTYLIDAE) W. R. Heyer,1 R. O. de Sá,2 and A. Rettig2 Keywords: Leptodactylus pentadactylus species cluster, advertisement calls, reproductive isolation, speciation. INTRODUCTION Herein we summarize the nature of the differentiation in- volved and discuss the evolutionary implications of our A recent re-evaluation of morphological and adver- findings. tisement call variation in the large species of frogs of the Leptodactylus pentadactylus cluster discovered more ex- amples of sibling species as defined by Ernst Mayr in his MATERIAL AND METHODS influential book Animal Species and Evolution. All previ- ously documented instances of sibling species in frogs Features for several color patterns, adult morphologi- demonstrated advertisement call differentiation consistent cal characters, and measurements were analyzed in terms with the calls serving as pre-mating isolating mechanisms. of geographic variation for the species currently known as However, we find one instance of two species with non- Leptodactylus knudseni, labyrinthicus, and pentadactylus distinguishable adult morphologies as well as non-distin- (Heyer et al., 2005). These data were used to postulate spe- guishable advertisement calls. Presumably, the new in- cies boundaries for the taxa studied. stances of sibling species reflect retention of ancestral Molecular sequence data were obtained for 1807 base adult morphologies and advertisement calls. Larval and pairs of 12S and 16S mitochondrial rDNA genes using habitat differentiation appear to be important factors in the standard techniques (see Heyer et al., in press). The speciation processes in this group of frogs. sequence data have GenBank accession numbers Ernst Mayr defined sibling species as, “morphologi- AY947855-82. Voucher specimen data are presented in the cally similar or identical natural populations that are re- Appendix. The sequence data were analyzed with maxi- productively isolated,” in his influential book Animal Spe- mum likelihood and parsimony methods using PAUP* cies and Evolution (Mayr, 1963 : 34). He considered the (Swofford, 1998). phenomenon to be important to understanding the com- plexity and scope of speciation processes in animals. Mayr’s concept of sibling species has been docu- RESULTS AND DISCUSSION mented in the frog genus Leptodactylus (Barrio, 1973; Heyer et al., 1996). In these examples, reproductive isola- Taxonomic Novelties tion among sibling species was documented through anal- ysis of advertisement calls. That is, advertisement calls are In order to discuss the biological implications of our very different from each other among species whose adults results it is necessary to give a brief synopsis of some of are morphologically identical. Females use the calls to dis- our taxonomic findings. A set of specimens from the State tinguish and select males of their own species to mate with of Pará, Brasil identified in collections either as L. knudse- in any mixed chorus where sibling species co-occur. ni or L. labyrinthicus represent a new species. This new In the process of re-evaluating variation in the Lepto- species will be referred to as the Pará species for purposes dactylus pentadactylus species cluster, we discovered in- of this paper. The taxon currently recognized as L. labyrin- stances of sibling species that do not demonstrate repro- thicus contains three species: L. labyrinthicus, L. vastus, ductive isolation on the basis of advertisement calls. and a new species from coastal Venezuela. Herein we use the available name L. vastus for the taxon occupying 1 Amphibians and Reptiles, MRC 162, PO Box 37012, Smithsonian Institu- northeastern Brazil (justification in Heyer, in press). The tion, Washington, DC 20013-7012, USA; E-mail: [email protected]. 2 Department of Biology, University of Richmond, Richmond, VA 23173, taxon currently recognized as L. pentadactylus consists of USA; E-mail: [email protected]. four species: L. pentadactylus and three new species re- 36 Herpetologia Petropolitana, Ananjeva N. and Tsinenko O. (eds.), pp. 35 – 39 4 5 3 2 0 1 0 –1 –5 Second Canonical Variable Second Canonical Variable –2 –3 –4 –10 –5 –4 –3 –2 –1 0 1 2 3 –10 –5 0 5 10 First Canonical Variable First Canonical Variable MiddleAmerica“pentadactylus ” L. bufonius Pacific Ecuador “pentadactylus ” L. elenae L. pentadactylus L. fuscus L. knudseni L. gracilis Pará L. latinasus L. labyrinthicus L. mystacinus L. vastus Fig. 1. Discriminant function analyses of male measurement data for comparable sets of species of the Leptodactylus pentadactylus species cluster (left) and the Leptodactylus fuscus group (right). The L. fuscus group species are those that occur together in the Gran Chaco of South America. Note that the data on the right are more structured than those on the left, for example, there is only a single cloud of points on the left and at least three clouds of points on the right and the sample confidence ellipses (p = 0.683) are much smaller on the right than the left. There are 6 confidence ellipses on the left (none for Pacific Ecuador “pentadactylus” with N = 3) and 6 on the right (the ellipses for L. fuscus and L. latinasus are not visible due to small sizes of ellipses and density of data points). ferred to herein as Middle American “pentadactylus,” Pa- so similar to those of L. labyrinthicus that it is likely that cific Colombia “pentadactylus,” and Pacific Ecuador females of any of these species would select males of the “pentadactylus.” The status of L. knudseni is unchanged. wrong species in a mixed chorus should they occur We analyzed DNA from all these species except for the sympatrically. coastal Venezuela and Pacific Colombia “pentadactylus” Although there is no adult morphological or advertise- species. ment call differentiation among certain of the species, Lack of Adult Morphological there are other features that are diagnostic. For example, and Advertisement Call Differentiation L. knudseni and Middle American “pentadactylus” differ from each other in several larval internal buccal cavity There is much less morphological differentiation characters as well as juvenile color patterns (Heyer, in among members of the L. pentadactylus cluster than found press). in other major clades of Leptodactylus studied to date. The measurement data illustrate the sort of differentiation ex- Genetic Relationships hibited by all the adult morphological data (Fig. 1). In par- ticular, adult morphologies can not distinguish L. knudseni The results of the mitochondrial rDNA gene analyses from Middle American “pentadactylus” nor L. labyrinthi- are best illustrated by the maximum likelihood bootstrap cus, L. vastus, and the northern Venezuela species from tree (Fig. 3) and the comparison of sequence differences each other (Heyer, in press). among the samples analyzed (Table 1). The advertisement calls of L. knudseni can not be con- Contrary to expectations based on the morphological sistently differentiated from the calls of Middle American and advertisement call data, neither L. knudseni/Middle “pentadactylus” (Fig. 2). The calls of these two species are American “pentadactylus” nor L. labyrinthicus/vastus are Herpetologia Petropolitana, Ananjeva N. and Tsinenko O. (eds.), pp. 35 – 39 37 100 msec 100 msec 2 2 1 1 Frequency, kHz Frequency, kHz 0 0 00.20.4 0 0.1 0.2 0.3 Time, sec Time, sec Leptodactylus knudseni MiddleAmerican“pentadactylus ” Fig. 2. Wave forms and audiospectrograms of Leptodactylus knudseni (USNM recording 228, cut 1) (left) and Middle American “pentadactylus” (USNM recording 106, cut 1) (right). The calls have the same duration, structure, and overlapping broadcast frequencies. sister-species in the molecular cladogram (Fig. 3) that re- tion within the L. pentadactylus cluster than observed in flects their genetic relationships. other major Leptodactylus clades. The variation includes differentiation in internal buccal cavity morphology, oral Sibling Species in Frogs Revisited disk morphology, and aquatic versus terrestrial larvae Our study demonstrates additional examples of sibling (Heyer, in press). Habitat differentiation is pronounced species as defined by Mayr (1963) in frogs of the genus among the species of the L. pentadactylus cluster in gen- Leptodactylus. Although sibling species in frogs are not eral and especially in those species lacking differences in common, they are not unexpected because they have been adult morphology or advertisement calls (Heyer, in press). documented in several families of frogs. We did expect to For example, L. labyrinthicus is closely associated with find that advertisement calls of sibling species in frogs the Cerrado Morphoclimatic Domain, L. vastus with the would serve as a reproductive isolating mechanism. Find- Caatinga Morphoclimatic Domain, whereas the morpho- ing sibling species that do not differ in advertisement calls logically similar Pará species occurs only within the rain but demonstrate extensive molecular differentiation has forests of the Amazonian Equatorial Morphoclimatic Do- not been previously reported in frogs that we are aware of. main as defined by Ab’Sáber (1977). There are two implications of our findings. Our study indicates that the role of advertisement calls 1) Ancestral adult morphologies and advertisement in frog speciation processes requires re-evaluation. We calls are retained
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