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Reproduction and Sexuality in Marine Fishes
Patterns and Processes
By Kathleen S. Cole
UNIVERSITY OF CALIFORNIA PRESSCopyright © 2010 the Regents of the University of California
All rights reserved.
John A. Musick
The chondrichthyan fishes have evolved separately from the Osteichthyes (Euteleostomi) since the dawn of gnathostomy more than 450 million years ago (Miller ; Kikugawa et al. 2004). Indeed, the chondrichthyans may be the oldest gnathostome group, perhaps having evolved from some thelodont agnathan ancestor in the Silurian (Marss et al. 2002). Whatever their origins, the Chondrichthyes and Osteichthyes underwent rapid divergent radiations during the Devonian (Miles 1967). This early divergence resulted in quite different reproductive trajectories in the two clades, probably initiated by high egg and larval predation from the newly evolved gnathostomes themselves (Musick & Ellis 2005). Osteichthyan reproductive evolution has been based on oviparity, with vulnerable ova lacking a maternally derived protective shell or case. Consequently, several adaptations have evolved multiple times to decrease egg predation (nest building, parental care, viviparity, etc.), or to maintain fitness despite predation (production of huge numbers of pelagic eggs). In contrast, chondrichthyan reproductive evolution has been based on lecithotrophic viviparity (i.e., yolk provides sole source of nutrients during development), matrotrophy (i.e., nutrients include maternally derived supplements), and in a small number of clades, oviparity with protective leathery egg cases. This chapter will review the evidence for this conclusion recently proposed by Musick & Ellis (2005).
THE CHONDRICHTHYAN REPRODUCTIVE SYSTEM
The elasmobranch reproductive system is predicated exclusively on internal fertilization. All male chondrichthyans have intromittent organs called claspers (myxopterygia), which are paired, grooved extensions of the posterior base of the pelvic fin, supported by cartilaginous endoskeletal elements (Compagno 1999).
Sperm is produced by the paired testes, then discharged into the ductus efferens and passed onto the convoluted epididymis, from which it passes on to the vas deferens and seminal vesicle (Conrath 2005)(Figure 1.1). The vas deferens and seminal vesicle function as storage areas for the semen, which may be packaged into spermatozeugmata or spermatophores (Wourms 1977). The paired seminal vesicles empty into a single urogenital sinus, which leads into a common cloaca. From there the semen enters the clasper grooves. Most male Chondrichthyes also posses siphon sacs, paired subcutaneous muscular bladders located just anterior to the base of the claspers. Each sac opens posteriorly through the apopyle and ends blindly anteriorly (Gilbert & Heath 1972). During copulation, the male usually inserts a single clasper into the female's urogenital opening and the siphon sac, which fills with seawater, functions under pressure to squirt semen into the female oviduct (Conrath 2005). The evolution of claspers has involved not only the coordinated development of the muscular siphon sac but also the muscles required to maneuver the clasper during copulation (Musick & Ellis 2005). The presence of claspers and prismatic skeletal calcification (i.e., a mineralized form of cartilage) are the two principal synapomorphies that define the Chondrichthyes (Grogan & Lund 2004). Thus, claspers and internal fertilization probably have been defining features of the group since its origin (Musick & Ellis 2005).
Prominent in both Figures 1.1 and 1.2 are the epigonal organs—long, white, strap-like bodies closely associated with the reproductive system in both sexes—however, epigonal organs are composed of myeloid tissue and are part of the immune system (Luer et al. 2004).
The female reproductive system (Figure 1.2) in Chondrichthyes is comprised of one or two ovaries, and paired oviducts into which the eggs enter through funnel-shaped ostia (Hamlett & Koob 1999). The oviducts pass into paired oviducal (=shell,=nidmental) glands. These are complex structures and histologically differentiated into four zones (Hamlett et al. 1998). Fertilization takes place in the anterior part of the oviducal glands, or just forward of them, in the oviduct. After an egg is fertilized, the oviducal gland surrounds the egg with a jelly coat and other egg investments and a tertiary egg envelope to form an egg capsule (Hamlett et al. 2005b). In many species, the oviducal gland may also store sperm in the posterior section from a few weeks to more than a year, leading to delayed fertilization after mating (Conrath 2005). The largest and most complex oviducal glands occur in oviparous species (Hamlett et al. 1998; Musick & Ellis 2005). Egg capsules pass out of the oviducal gland through the isthmus to the paired uteri. Function of the uteri varies depending on the reproductive mode of the species at hand. In yolk-sac viviparous and oophagous species, the uterus regulates the uterine environment; supplies oxygen, water, and minerals; and regulates wastes (Hamlett & Koob 1999). In other matrotrophic viviparous species, the uterus provides the above services, but it also produces nutritious mucous in limited histotrophs, and copious uterine "milk" in lipid histotrophs, and is the site of embryonic placentation in placental species (Hamlett & Hysell 1998). The uterus in oviparous species contributes to polymerization and scleratization of the egg capsule, which may be retained for several days before oviposition (Hamlett & Hysell 1998).
The uteri unite posteriorly to form a cervical and urogenital sinus (Hamlett & Koob 1999), which empties into the cloaca. In many species of viviparous sharks, only the right ovary develops, but the rest of the reproductive system is paired (Conrath 2005). Conversely, in many myliobatid rays, the entire reproductive system on the right side may be reduced.
CHONDRICHTHYAN MODES OF REPRODUCTION
Although the extant chondrichthyans are a relatively small class of vertebrates, including about 1100 species of elasmobranchs (sharks and rays) and 30+ species of holocephalans (chimaeras), they exhibit a surprising diversity of reproductive modes (Hamlett et al. 2005b).
These modes may be classified into lecithotrophic and matrotrophic based on whether fetal nutrition is supported solely by the yolk in the egg or augmented by additional maternal input of nutrients during development (Wourms 1981)(Table 1.1). Lecithotrophy includes two forms of oviparity (single and multiple) and one form of viviparity (yolk sack viviparity). Matrotrophy includes five different forms of viviparity (Wourms 1981; Hamlett et al. 2005b; Musick & Ellis)(Table 1.1).
Oviparous chondrichthyans all deposit benthic eggs with leathery, structurally complex shells (Hamlett & Koob 1999). Chondrichthyan oviparity is limited to clades that are benthic in habit. Single oviparity, in which eggs are usually deposited on the sea floor in pairs, one from each uterus, is the only form of reproduction in the extant holocephalans. However, this group is but a small relic of a once diverse group of Mississippian chondrichthyans within which viviparity has been well documented in different taxa (Lund 1980, 1990; Grogan 1993, 2000, 2009, unpublished data). Evidence of oviparity is sparse in the Bear Gulch, the most intensively studied Mississippian fossil deposit, despite the high quality of preservation there (Grogan & Lund 2004). Within the elasmobranchs, oviparity occurs in only a small number of clades (some speciose).
Single oviparity is the sole form of reproduction in the horn sharks (Heterodontiformes), the batoid family Rajidae (skates), and in most cat sharks (Scyliorhinidae) and occurs along with various forms of viviparity in the carpet sharks (Orectolobiformes). In single oviparity, eggs are usually deposited every few days over a period of months. This results in an annual fecundity of 20 to 100 or more eggs per year in most species (Musick & Ellis 2005), an order of magnitude higher than that of viviparous elasmobranchs of similar size. Oviparity in elasmobranchs has evolved as an adaptation to increase fecundity in groups in which most members have small body size (<100cm TL) and thus limited uterine capacity (Musick & Ellis 2005). In addition, oviparity in small elasmobranchs may represent a form of "bet hedging" (Stearns 1992). Small individuals suffer a proportionally higher predation rate than do large individuals (Cortés 2004). If a pregnant viviparous shark is eaten, her immediate fitness is zero, whereas if an oviparous species is predated, her most recently produced offspring may still survive (Frisk et al. 2002; Musick & Ellis 2005). Multiple oviparity (Table 1.1) occurs in a small number of Scyliorhinidae and represents an evolutionary reversal. In this reproductive mode, females retain developing eggs in the uterus for most of the developmental period, then deposit them before they hatch (Nakaya 1975). This obviously limits the fecundity and probably has evolved in response to very high egg predation rates (Musick & Ellis 2005). The same may be said about a small number of scyliorhinids in the terminal sub-tribe Galeini, which have reverted to yolk-sac viviparity (Musick & Ellis 2005).
Yolk-sac viviparity is the simplest form of viviparity, wherein the developing eggs are retained within the uterus until parturition and fetal nutrition is supplied solely by the yolk and thus is lecithotrophic (Hamlett et al. 2005b). This form of reproduction is basal and most widespread in elasmobranchs and is present in all extant orders except the Heterodontiformes, which are oviparous, and the Lamniformes, which have a more advanced form of viviparity (oophagy)(Musick & Ellis 2005)(Figure 1.3). Yolk-sac viviparity occurs in many species formally classified as "ovoviviparous." The term ovoviviparous was abandoned because some of the species so classified actually exhibited a limited form of matrotrophy (Ranzi 1934; Budker 1958; Hoar 1969). Subsequently, "ovoviviparity" was replaced by the term "aplacental viviparity," which included three major modes of elasmobranch reproduction (yolk-sac viviparity, histotrophy, and oophagy), thus obscuring the true reproductive diversity in the group. In addition to being based on a negative attribute (lack of a placenta), by inference, the term elevated the relative importance of placental viviparity, a mode of reproduction restricted to a small number of terminal nodes within the Carcharhiniformes (Musick & Ellis 2005). The term "aplacental viviparity" should be abandoned and replaced with "yolk-sac viviparity," "histotrophy," or "oophagy" as appropriate.
Mucoid (Limited) Histotrophy. Mucoid histotrophy is the simplest form of matrotrophic viviparity wherein developing embryos receive additional nutrients above those supplied in the yolk (Hamlett et al. b; Musick & Ellis 2005) by ingesting mucus produced by the uterus. This form of matrotrophy may be insidious and difficult to detect without obtaining ash-free dry weights from newly fertilized ova to compare with those of full -term embryos (Ranzi 1934; Needham 1942, Hamlett et al. 2005b). During embryogenesis, nutrients are expended to support the metabolic requirements for embryonic maintenance, growth, and development. Thus, in truly lecithotrophic species, more than a 20 percent reduction of ash-free dry weight should occur during development from egg to term embryo (Hamlett et al. 2005b). Ranzi (1932, 1934) noted early on that although some lecithotrophic species of Torpediniformes and Squaliformes lost 23 to 46 percent organic content during development, other squaliforms and some Triakidae supposed to be lecithotrophic actually gained 1 to 369 percent in organic content. Evidence for mucoid histotrophy may also be provided by histological examination of the uterine walls, which should exhibit high mucus secretory activity at least during early and midterm development (Hamlett et al. 2005b). Mucoid histotrophy appears to be widespread among viviparous groups, and further research is needed to determine the frequency of this reproductive mode (Hamlett et al. 2005b).
Lipid Histotrophy. Lipid histrophy is restricted to the myliobatiform stingrays. This reproductive mode involves the secretion of a lipid-rich histotroph from highly developed secretory structures called trophonemata located in the uterine lining. Embryos supported by lipid histotrophy may undergo an increase in organic content of 1980 to 4900 percent (Needham 1942).
Oophagy. Oophagy is a form of matrotrophic viviparity where embryonic development is supplemented by the mother's production of unfertilized eggs, which are ingested by the embryo. (Musick & Ellis 2005). This nominal mode of reproduction has evolved twice among elasmobranchs: in the lamniforms, and in the small carcharhiniform family, Pseudotriakidae. The mechanics of oophagy in these two groups differ and are not homologous (Musick & Ellis 2005). Oophagy is the only mode of reproduction known in the lamniforms, where large numbers of unfertilized eggs are produced by the mother and ingested by the embryos during most of the pregnancy (Gilmore et al. 2005). Adelphophagy (intrauterine cannibalism), where the first embryo that develops in each uterus attacks and eats its developing siblings, is an extension of oophagy and is known to occur in only one species, the sand tiger (Carcharias taurus). After the embryos have eaten their siblings, subsequent development in this species is supported through oophagy, as in all other Lamniformes (Gilmore et al. 2005). Adelphophagy results in the birth of only two large (>1m TL) neonates, one from each uterus.
In the carcharhiniform Pseudotriakidae, a number of unfertilized eggs are included within the egg envelope with the embryo, which then ingests the eggs during development. No further unfertilized eggs are produced to support the developing embryos above those included in the egg envelope, but the Pseudotriakidae may also be limited histotrophs (Yano 1992, 1993).
Placental Viviparity. Placental viviparity is present in five higher families within the Carcharhiniformes. The "placenta" in elasmobranchs is analogous, but not homologous, to that in mammals and has been termed a yolk-sac placenta (Hamlett et al. 2005b). In elasmobranchs, the yolk sac forms the attachment with the uterine epithelium and the yolk stalk elongates to form an umbilical cord. The developing embryos are maintained in separate uterine compartments. All placental sharks utilize yolk stores from the egg for initial development, and then mucoid histotrophy before, and for some species, even during placentation (Hamlett 1989; Hamlett et al. 2005b).
The Neoselachii are a monophyletic sub-class that includes all living elasmobranchs as well as some extinct Mesozoic forms and possibly, a small number of Paleozoic fossils (Maisey et al. 2007). Historical classifications of modern elasmobranchs have recognized two major clades: the Batoidei and the Selachii (Bigelow & Schroder 1948, 1953). This classification was radically changed in the 1990s following morphological cladistic analyses that placed the Batoidei as a terminal group within the squalomorph sharks in a new clade, the Hypnosqualea (Shirai 1992, 1996; de Carvalho 1996), an arrangement that was in conflict with the paleontological data. The earliest known batoids had separated from and were concurrent with the earliest heterodontiform, hexanchiform, and orectolobiform sharks by the Jurassic if not earlier (Thies 1983; Capetta 1987; Maisey et al. 2007), contradicting the batoid terminal position in the cladistic analysis. This contradiction was resolved by more recent molecular and paleontological analyses (Douady et al. 2003; Naylor et al. 2005; Maisey et al. 2007), which clearly showed the Batoidei to be the sister group to the Selachii. Cladistic misclassification of the Batoidei based on morphology may have been mitigated by homoplasies shared by the benthic, dorsoventrally flattened batoids and the squalean Squantiniformes (Nelson, 2006).
Excerpted from Reproduction and Sexuality in Marine Fishes by Kathleen S. Cole. Copyright © 2010 the Regents of the University of California. Excerpted by permission of UNIVERSITY OF CALIFORNIA PRESS.
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Table of Contents
Introduction Kathleen S. Cole, xv,
PART ONE. PATTERNS,
1. Chondrichthyan Reproduction John A. Musick, 3,
2. Reproduction and Development in Epipelagic Fishes Bruce B. Collette, 21,
3. Reproduction in Scorpaeniformes Marta Muñoz, 65,
4. Parental Care, Oviposition Sites, and Mating Systems of Blennioid Fishes Philip A. Hastings and Christopher W. Petersen, 91,
5. Gonad Morphology in Hermaphroditic Gobies Kathleen S. Cole, 117,
PART TWO. PROCESSES,
6. Gonad Development in Hermaphroditic Gobies Kathleen S. Cole, 165,
7. Fertilization in Marine Fishes Christopher W. Petersen, 203,
8. Bidirectional Sex Change in Marine Fishes Philip L. Munday, Tetsuo Kuwamura, and Frederieke J. Kroon, 241,
9. Neuroendocrine Regulation of Sex Change and Alternate Sexual Phenotypes in Sex-Changing Reef Fishes John Godwin, 273,
10. Acoustical Behavior of Coral Reef Fishes Phillip S. Lobel, Ingrid M. Kaatz, and Aaron N. Rice, 307,
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