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Phylogenetic and Habitat Influences on Mating System Structure in the Humbug Damselfishes (Dascyllus, Pomacentridae)

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Phylogenetic and Habitat Influences on Mating System Structure in the Humbug Damselfishes (Dascyllus, Pomacentridae) BULLETIN OF MARINE SCIENCE. 57(3): 637~52. 1995 PHYLOGENETIC AND HABITAT INFLUENCES ON MATING SYSTEM STRUCTURE IN THE HUMBUG DAMSELFISHES (DASCYLLUS, POMACENTRIDAE) John Godwin ABSTRACT The darnselfish genus Dascyllus contains nine species and exhibits protogynous sex change and/or functional gonochorism with variation both interspecifically and possibly intraspecif- ically between habitats. The genus can be divided into three species complexes and along lines of both descent and body size: 1) five species in two species complexes (complexes I and 2) are relatively small-bodied, closely associate with branching coral throughout life, and commonly exhibit resource defense polygyny and associated protogynous sex change, 2) three species in a third species complex (complex 3) reach larger body size, closely associate with branching coral only as juveniles, and do not exhibit resource defense polygyny, and 3) D. ftavicaudus, a large-bodied member of the otherwise small-bodied species complex 2. Das- cyllus ftavicaudus and D. albisella (complex 3) are both large bodied, but differ in their responses to habitat type. Dascyllus flavicaudus shows differences in sex ratio, space use and mating system between a discontinuous coral cover habitat (female-biased sex ratio, resource defense polygyny) and continuous coral cover habitat (non-biased sex ratio, no resource defense polygyny) while D. albisella does not (non-biased sex ratio, no apparent resource defense polygyny in either habitat type), suggesting that both ecological factors and phylo- genetic history influence these characters. Emlen and Oring (1977) proposed that the dispersion of resources critical to the limiting sex, usually females, is a major determinant of mating system struc- ture. Males monopolizing critical resources may also gain exclusive mating access to females (resource-defense polygyny), giving such males high reproductive suc- cess. However, phylogenetic history can be very important in shaping and con- straining adaptation. It has become increasingly apparent that modern character states such as mating system responses to ecological factors can be profitably considered in a phylogenetic context (Brooks and McLennan, 1991). This paper concerns variation in mating system structure in a genus of Indo- Pacific damselfishes, the Dascyllus. The Dascyllus consists of nine species dis- tributed across the tropical Indo-Pacific from the Red Sea to Hawaii (Fig. la-c; Randall and Allen, 1977). These small planktivores all exhibit a strong association with live branching coral during at least the juvenile stage of their life history. The eggs are demersal and parental care is provided solely by males. This is one of the better studied genera of coral reef fishes and has been the subject of ap- proximately 40 papers including many related to reproductive and feeding ecol- ogy, mating and social behavior, and protogynous sex change (in addition to papers cited below: see: Holzberg, 1973; Jones, 1988; Sale, 1971a, 1971b, 1972a, 1972b, 1976; Shpigel and Fishelson, 1983; Sweatman, 1983, 1985, 1988). The genus can be divided into three species complexes on the basis of mor- phology, biogeography, and striking coloration differences (affinities and character similarities described in Randall and Allen, 1977). I will refer to these as the aruanus, reticulatus, and trimaculatus complexes respectively (groups 1-3 from abstract) for the most geographically widespread member species of each (Fig. 1, aruanus complex: D. aruanus, D. melanurus; reticulatus complex: D. reticulatus, D. cameus, D. marginatus, D. fiavicaudus; trimaculatus complex: D. trimaculatus, D. albisella, D. strasburgi; Fig. 2). 637 638 BULLETIN OF MARINE SCIENCE, VOL. 57, NO, 3, 1995 aruanus complex '::, ··:9::::::::::::::::::::::::::-:·:···· -, reticulatus complex .-:.. .-:0-:·:-:-:-:-:·:-:-:-:-:-:·:-:-:-'·'. .. - . trimaculatus complex " > D. strasburgi Figure 1. Distributional maps for species complexes within the genus Dascyllus. The reticulatus and aruanus complexes are both small-bodied, reaching maxi- mum sizes of approximately 65-70 mm SL. The exception is D. flavicaudus, a member of the reticulatus complex which reaches at least 90 mm SL. The three species of the trimaculatus complex reach greater maximum body sizes (100-110 GODWIN: MATING SYSTEMS IN DASCYLLUS DAMSELFISHES 639 species body size sex change Figure 2. Hypothesized relationships between Dascyllus species complexes. Body size: "I.:'-large bodied, "s"-small bodied; Sex change: "y"-species exhibits sex change, "n"-species has been studied but functional sex change has not been described, ?-species has not been studied. (*Diagnosis of sex change in D. flavicaudus is from this paper). mm SL). This length difference represents an approximate four to fivefold dif- ference in body mass. Both protogynous hermaphroditism and apparent functional gonochorism are exhibited in the Dascyllus. Protogynous sex change was first documented for the genus in D. aruanus (Fricke and Holzberg, 1974; Coates, 1982) and subsequently in two members of the reticulatus complex, D. reticulatus (Schwarz, 1980; Schwarz and Smith, 1990) and D. marginatus (Shpigel and Fishelson, 1986). Functional protogynous sex change has not been described in the trimaculatus complex despite some study of social systems and ecology in D. trimaculatus and D. albisella (Stevenson, 1963; Barash, 1980; Godwin, this paper). No published information is available for D. carneus, D. strasburgi, or D. melanurus, although in Madang, Papua New Guinea D. melanurus appears to have a similar social organization to D. aruanus and thus probably exhibits sex change (pers. obs.). Functional protogynous sex change in Dascyllus species appears to be associated exclusively with a haremic polygynous mating system in which males defend coral heads on which females are resident (Fricke and Holzberg, 1974; Coates, 1982; Schwarz and Smith, 1990; Shpigel and Fishelson, 1986). For purposes of this paper, sex change is considered primarily as a consequence of this type of mating system. Elsewhere (Godwin, in prep.), I describe an unusual form of sex change (intermediate between pre- and post-maturational) in D. albisella and more directly address the evolution of sexual patterns in the genus. Based on findings to date, the distribution of resource defense polygyny and sex change in the Dascyllus fall along lines of both body size and descent (Fig. 2). Relationships among the three species complexes are not known. The rela- tionships among species complexes depicted in Figure 2 are based on the inter- pretation of meristic character data which follows (data from Randall and Allen, 1977). These data suggest two alternate topologies depending on the characters used. Similarities in modal numbers of pectoral rays and especially soft dorsal rays suggest a closer relationship between the reticulatus and trimaculatus com- plexes, while modal gill raker counts on the first arch suggest a closer relationship between the aruanus and trimaculatus complexes. However, comparisons of gill raker counts between species are confounded by an influence of body size. In 640 BULLETIN OF MARINE SCIENCE, VOL. 57, NO.3, 1995 examining correlations between meristic characters within individuals (raw data provided by H. Randall and G. Allen), I found significant positive relationships between standard length and gill raker counts within several Dascyllus species: D. aruanus (upper limb gill rakers: r = 0.252, P < 0.001; lower limb gill rakers: r = 0.175, P = 0.007, N = 241), D. reticulatus (upper limb gill rakers: r = 0.020, P = 0.833, lower limb gill rakers: r = 0.362, P < 0.001, N = 112), D. trimaculatus (upper limb gill rakers: r = 0.532, P = 0.012, lower limb gill rakers: r = 0.624, P = 0.002). Gill raker counts therefore do not appear to be useful indicators of phylogenetic relationships in Dascyllus. No significant correlations were found between standard length and either soft dorsal or pectoral ray counts for any Dascyllus. These data therefore tentatively support an initial separation between the aruanus complex and the lineage leading to the rcticulatus and tri- maculatus complexes, followed by a later separation of the reticulatus and tri- maculatus lineages (Fig. 2). While more data are clearly necessary to firmly re- solve the subgeneric relationships here, the important point for purposes of this study is the relationship that is not supported: a closer affinity between the aruanus and reticulatus complexes than between either complex and the trimaculatus com- plex. Taken together, these data suggest that the ancestral Dascyllus was small- bodied and sex changing. This would require one transition to produce the large- bodied trimaculatus complex rather than two transitions from a large-bodied an- cestor to produce the predominantly small-bodied aruanus and reticulatus com- plexes. I propose two alternative hypotheses here to account for the observed patterns of body size and sex change in Dascyllus. These hypotheses were proposed a posteriori for most of the genus as information was available for D. aruanus, D. reticulatus, D. marginatus, D. trimaculatus, and D. albisella. Information was not available for D. flavicaudus and predictions were therefore a priori with respect to this critical test species. Individuals of small Dascyllus species are typically restricted to coral heads where these heads are spatially separated. This restricted mobility has been as- cribed to predation pressure limiting movement between corals (Fricke,
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