Extremely early maturity found in Okinawan gobioid fishes Takeshi Kon** and Tetsuo Yoshino Department of Marine Sciences, Faculty of Science, University of the Ryukyus, 1 Senbaru, Nishihara Okinawa 903-0213, Japan (e-mail: TY,
[email protected]) * Present address: Department of Marine Bioscience, Ocean Research Institute, University of Tokyo, 1-15-1 Minamidai, Nakano, Tokyo 164-8639, Japan (e-mail:
[email protected]) Received: September 27, 2001 / Revised: January 26, 2002 / Accepted: February 20, 2002
Ichthyological Research ©The Ichthyological Society of Japan 2002
Ichthyol Res (2002) 49: 224–228
Abstract Extremely small animals including fishes have been reported with discussion of the causes and consequences of their miniaturization. Here we demonstrate, for the first time, very early (i.e., 23–60 days old and 42–67 days old) sexual maturity in two groups of gobioid fishes (Schindleria and Paedogobius, respectively) in warm water, based on the otolith increments. The generation time of Schindleria is the shortest known among vertebrates under natural conditions. We discuss the occurrence and evolutionary significance of the progenesis found in gobioid fishes. Key words Gobioidei · Progenesis · Warm waters · Otolith · Daily increments
W
hat is the smallest vertebrate? Many biologists have reported extremely small animals, including fishes from Southeast Asia (Roberts, 1986; Parenti, 1989), South America (Roberts, 1984; Weitzman and Vari, 1988), and Africa (Grande, 1994), and have discussed the causes and consequences of their miniaturization (Hanken and Wake, 1993; Miller, 1996). Miniaturization is assumed, without substantial age data (especially in fish), to accompany early maturity (or progenesis in paedomorphosis) being one of the effective strategies for the increase of r (Gould, 1977). In addition, early maturity is expected to accelerate speciation, leading to an increase in species taxonomic diversity (Marzluff and Dial, 1991; Munday and Jones, 1998). The suborder Gobioidei (Teleostei, Perciformes) comprises more than 2000 species that are distributed worldwide and adapted to various environments. Of these, some progenetic gobioids, Schindleria spp. and Paedogobius kimurai, are known to inhabit coral reefs and muddy bottoms, respectively, in the Ryukyu Islands. The two species of the gobioid genus Schindleria, S. praematura and S. pietschmanni, broadly distributed in coral reefs of the Indo-Pacific region and characterized by a slender translucent body and absence of the first dorsal and pelvic fins, are known as one of the smallest vertebrates in the world (Johnson and Brothers, 1993). In Okinawa Island, Schindleria is observed throughout the year, and one type of female similar to S. praematura in having 17–22 dorsal fin rays, 10–13 anal fin rays, and a urogenital papilla with two projections is very common. We herein call the female as Schindleria type 1. Another species, Paedogobius kimurai, is a diandric goby distributed in the Ryukyu Islands, Thailand, and Australia (Neira et al., 1998; Iwata et al., 2001). The female is planktonic, lacking a pelvic fin, whereas the secondary male is benthic, having a pelvic fin and a large mouth with strong canine-like teeth.
In recent years, many studies have demonstrated that the examination of otolith microstructure and counting of daily growth increments allow the age of individual fish, including that of gobioid fishes, to be determined with great precision (Campana and Neilson, 1985; Iglesias et al., 1997; Hernaman et al., 2000). Using this method, we obtained convincing data for the age of maturity in Schindleria type 1 and P. kimurai in Okinawa I. and thereby estimated the generation time for the first time. We then compared generation times between progenetic and neotenic gobioids in relation to seasonal trends in water temperature and, especially in Schindleria type 1, discuss the bearing of shortened generation time on the species diversification as recognized.
Materials and Methods Sampling materials.—Examined specimens of Schindleria type 1 were collected at high tide of every month (new moon) from June 1999 to July 2000, at Motobu, Okinawa I., Ryukyu Is., by hand net or bucket with a night lamp. We examined 131 ripe specimens of Schindleria type 1 (of 1209 specimens of Schindleria spp.). Paedogobius kimurai were collected on 21 May 1998 and 12 February 2000, at Nakagusuku Bay, Okinawa I., by seine net. The seine net, which consisted of two 56-m-long wings and a 24-m-long ⫻ 10-m-high ⫻ 11-m-wide pocket, was fished to a depth of about 10 m and swept an area of about 1700 m2. We examined 7 ripe specimens (of 23 specimens). Sex and developmental stage of gonads were determined by direct observation of ovarian eggs visible through the translucent body wall. Records of surface water temperature in the study sites were obtained from JODC (Japan Oceanographic Data Center) as monthly averages between 1906 and 1994 at the western coast of Okinawa Island.
Progenesis of Okinawan gobioids
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Counting increments of the otolith.—All specimens were preserved in 95% ethanol after measuring standard length (measured directly between the tip of the snout and the base of the caudal fin). Right and left sagittal otoliths were removed from each side of the cranium. Increment readings were carried out under a light microscope (400–900⫻). The increments were read along the longest radius of the otolith from the primordium to the margin, until counts coincided three times. When different counts were gained between right and left otoliths, the highest was accepted as the age in days for each specimen. This age obtained is an approximation, as it was unknown when the formation of the increments began. The count lacks a correction factor corresponding to the period between fertilization and the formation of the first increment. This time lag seems, however, to be less than a few days, because formation of the first increment in some fishes coincides with the eye pigmentation stage (Watanabe, 1997), which usually occurs 3 days after fertilization in gobioid fishes at warm temperature (reviewed in Kon and Yoshino, 2002). Daily incremental formation of otoliths was unsuccessful to marking the otoliths with alizarin complexon (ALC) to validate the periodicity of deposition, because Schindleria and Paedogobius were very susceptible to sampling stress, and all samples died immediately.
Results The sagittal otoliths of Schindleria type 1 were disc-shaped in many specimens and slightly oval in some specimens (Fig. 1A). Ages at maturity and standard lengths (SL) of examined Schindleria type 1 are shown in Fig. 2. The increment counts ranged between 23 (in June and July) and 60 (in March). Earlier maturity occurred between June and August (av 31 and 28 days old, respectively). The older age at maturity (av 39.7–42.7 days) tended to increase between January and April. Thus, Schindleria type 1 (female) is considered to mature at about 28–43 days old (av 37.1), attaining more than 16–18 mm SL every month, and its alternation of generations was estimated at more than nine times per year. The sagittal otoliths of Paedogobius kimurai were slightly concave-convex in form and disc-shaped (Fig. 1B). The increment counts ranged between 42 and 59 (12.2– 13.9 mm SL) in May and were 67 (16.1 mm SL) in February (Fig. 3). The size and age in February specimens was much increased compared to those in May. Consequently, the alternation of generations of the P. kimurai (female) was estimated at about six times per year.
Discussion Heterochrony, including paedomorphosis, has become one of the focal concepts of evolutionary biology in the past 25 years (Reilly et al., 1997; Klingenberg, 1998). It is important to note that evolution with large modifications may be achieved by heterochrony, owing to the dissolution of
Fig. 1. Sagittal otoliths of ripe specimens in progenetic gobioids from Okinawa Island. A Schindleria type 1, 16.4 mm standard length (SL). Light photomicrograph shows 31 increments. B Paedogobius kimurai, 13.3 mm SL. Light photomicrograph shows 42 increments
conflict between developmental constraints and adaptive evolution. Paedomorphosis, or the retention of ancestral juvenile characters by later ontogenetic stages of descendants, is categorized into two major types with life history strategies, “progenesis” (truncation of somatic development with early maturity) and “neoteny” (slower somatic development) (Gould, 1977; Alberch et al., 1979). Recently, Reilly et al. (1997) introduced the alternative heterochronical terminology, i.e., “hypomorphosis (with early maturity)” for progenesis and “deceleration” for neoteny; however, the present study used Gould’s traditional terminology to provide a simple explanation in our discussion. To judge the type of paedomorphosis, it is necessary to estimate the
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Fig. 2. Monthly change in water temperature between 1906 and 1994 (upper), age at maturity (middle), and standard length (lower) of Schindleria type 1. Arabic numerals, number of specimens examined
Fig. 3. Relationship between number of daily growth increments in sagittal otolith and standard length in Paedogobius kimurai. Solid circles, mature specimens in May 1998; open circles, immature specimens in May 1998; solid triangle, a mature specimen in February 2000
phylogeny of targeted taxa and determine the polarity of relevant developmental characters. However, phylogeny within Gobioidei is difficult to estimate, because paedomorphic fishes, especially Schindleria, have reduced characters that are difficult to compare with other species. Moreover, molecular data indicate that many gobioids have diverged almost simultaneously or during an extremely short period (Akihito et al., 2000). According to Iwata et al. (2001), Paedogobius belongs in the Gobiopterus group sensu Birdsong et al. (1988);
T. Kon and T. Yoshino
Fig. 4. Ontogenetic trajectories of two paedomorphic gobioids from Japan. A Progenesis in Schindleria (⫽hypomorphosis with early maturity); B neoteny in Leucopsarion (⫽deceleration with same age at maturity), compared with ontogeny of plesiomorphic gobioids
however, early life histories in the group are unknown. We inferred the plesiomorphic ontogeny of gobioids, including eleotrids (sensu Hoese, 1984; Hoese and Gill, 1993), on the basis of available published information, as several months planktonic-larval duration (age at full complement of fin rays) and sexual maturity at 6–12 months (e.g., Dotsu and Fujita, 1959; Auty, 1978; Miller, 1984; Shiogaki and Dotsu, 1988; Bell et al., 1995; Shen et al., 1998). In comparison with this plesiomorphic ontogeny, Schindleria type 1, maturing in 23–60 days, and lacking first dorsal and anal fins, are thus regarded as progenetic (Fig. 4A). The ontogeny of Paedogobius kimurai also indicates a progenetic tendency, according to maturity between 42 and 67 days. The progenetic gobioids, Schindleria and Paedogobius, are distributed in warm waters, whereas two other paedomorphic gobies from temperate or cold waters, Leucopsarion petersii (lacking first dorsal fin and having reduced pelvic fin) (Dotsu and Uchida, 1979) and Crystallogobius linearis (lacking first dorsal fin and having reduced or lacking pelvic fin in female) (Miller, 1986), mature no earlier than 1 year old and thus are considered neotenic (Fig. 4B). In addition, the European gobies Pseudaphya ferrei (see Miller, 1973) and Aphia minuta (see Iglesias et al., 1997; Caputo et al., 2000), which show a greater morphological development than the above two neotenic species and mature at 1 year (some individuals of the latter species at several months), may also be considered as showing a neotenic tendency compared with plesiomorphic ontogeny.
Progenesis of Okinawan gobioids
Why do different types of paedomorphosis occur between tropical and temperate-cold water gobioid fishes? Difference of age at maturity between two types of paedomorphosis has resulted from abiotic and biotic factors. Temperature influences the rate of all metabolic processes, and so for ectothermic animals such as fish there is invariably a relationship between environmental temperature and the metabolically demanding process as related to reproduction (Bye, 1990). Warmer temperature accelerates gonadal development within the species (Yamazaki, 1965; Yoshioka, 1970); however, progenesis by early maturity does not occur in warm temperatures unless hatched larvae are able to survive. In addition, for most species, maturity and spawning occur within a relatively narrow preferred temperature range under natural conditions (Bye, 1990). Therefore, the occurrence of progenesis is not always necessary for gonadal maturity directly accelerated by warm temperature. However, “stable” warm temperature should indirectly affect timing of maturity in relation to survival of fish larvae. From previous reports, it is conceivable that a single principal factor determines these two aspects of paedomorphic ontogeny with maturity. The availability of zooplankton as food for fish larvae in tropical environments is much more stable throughout the year than that in temperate-cold waters because it is low in winter (Cushing, 1990). For example, many individuals of the European “common goby,” Pomatoschistus microps, attain a suitable size for sexual maturity by the first winter of life, although reproduction does not begin until the following March and April (Miller, 1975; Fouda and Miller, 1981). Many studies have shown that tropical waters are characterized by environmental conditions resulting independently in small progenetic fishes as follows: Tyson (Perciformes; Gobioidei) (Springer, 1983), Sundasalanx (Clupeiformes) (Siebert, 1997), Phallosttethus (Atheriniformes) (Parenti, 1989), and Danionella (Cypriniformes) (Roberts, 1986) from Southeast Asia and Amazonsprattus (Clupeiformes) (Roberts, 1984) from South America. On the other hand, paedomorphic salangid fishes (Osmeriformes) distributed in temperate or cold Asian waters, attaining 60–150 mm, are neotenic in tendency because of maturity at 1 year, the same age as their ancestral relatives (Saruwatari, 1994; Zhang and Qiao, 1994). It is suggested that paedomorphic ontogeny of descendants expressed as progenesis or neoteny is constrained by seasonally restricted maturity. This hypothesis is supported by experimental results showing that a blennid fish Dasson trossulus spawned at 95 days in aquarium with abundant food and a stable environment although it matures at 1 year in the wild condition (Dotsu, 1982). In the genus Schindleria, two species have been identified only by the relative positions of the dorsal and anal fins without further morphological comparison. In the males, however, the morphology of the urogenital papillae exhibits extensive variation. The combination of several morphological characters, including shape of the urogenital papilla and the numbers of dorsal and anal fin rays and myomeres, indicates that there are actually no fewer than eight species in Okinawa I., none of which are identified with previously
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described species (Yoshino et al., 2000). However, correspondence of Schindleria type 1 to the species discriminated by males remains unresolved. We suspect that Schindleria contains many species in each portion of the Indo-Pacific region. The generation time of Schindleria type 1 (av 37.1 days, nine times of alternation per year) is one of the shortest among vertebrates (cf. pygmy mice, which mature at more than 50 days after fertilization) (Nowak, 1991). The rapid alternation of generations should produce more genetic variation by enhancing recombination of genes (Martin and Palumbi, 1993). The short generation time is thus expected to contribute to an increase in speciation and diversity of a given lineage (Marzluff and Dial, 1991). Therefore, the diversity of Schindleria may be related to its short generation time. Progenesis by truncation of development was pointed out as one of the few processes that can lead to the unbinding of morphology in macroevolution (Gould, 1977). However, the rapid alternation of generation in progenesis occurring in warm stable waters also should play an important evolutionary role. Acknowledgments We sincerely thank T. Shimojo (Okinawa Prefectural Fisheries Experimental Station), T. Uyeno and M. Manabe (National Science Museum, Tokyo), K. Tachihara, R. van Woesik, and H. Ota (University of the Ryukyus) for comments on the manuscript, and N. Takei, A. Hayashi, and H. Ishimori (University of the Ryukyus) for assistance with sample collection.
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