13
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
The Phylogeny of
Atherinomorphs:
Evolution of a
Novel Fish
Reproductive
System
Lynne R. Parenti
Division of Fishes, MRC NHB 159, Department of
Vertebrate Zoology, National Museum of Natural History,
Smithsonian Institution,
Washington, DC, USA.
14 ? Viviparous Fishes Systematics, Biogeography, and Evolution
The Phylogeny of
Atherinomorphs:
Evolution of a
Novel Fish
Reproductive
System
Lynne R. Parenti
Abstract
The fishes commonly known in English as
silversides, rainbowfishes, phallostethids,
killifishes, ricefishes, halfbeaks, needlefishes,
flying fishes, and sauries were combined by
Rosen (1964), into one taxon, now known as
the Atherinomorpha, largely using osteological
and reproductive characters. Subsequent
reviews have supported atherinomorph
monophyly, adding characters to the
diagnosis. Today atherinomorphs are
diagnosed as monophyletic by derived
characters of the testis, egg, reproductive
mode, circulatory system, jaw musculature,
olfactory organ, and various parts of the
skeleton including the ethmoid region of the
skull, gill arches, pelvic girdle, among others.
Support for monophyly of each of the three
included taxa, now classified as the orders
Cyprinodontiformes, Beloniformes, and
Atheriniformes, and the relationships among
them, varies in quantity and quality. During
the past twenty years, reproductive and
molecular data used to infer atherinomorph
relationships have grown significantly. In
general, molecular data support hypotheses
based on morphology, and, in some cases,
provide novel hypotheses and unique
challenges to morphological data. A growing
body of data indicates that all atherinomorphs
share a unique testis-type that is correlated
with an array of reproductive modifications
such as coupling during mating, relatively
long developmental period, sperm-bundle
formation, internal fertilization, superfetation,
embryo retention, diapause, delayed hatching,
hermaphroditism, and live-bearing.
Corroboration of an atherinomorph sister
group may include identification of some
unique aspects of this reproductive system in
other taxa.
Resumen
Los peces com?nmente conocidos en ingl?s
como: silversides, rainbowfishes, phallostethids,
killifishes, ricefishes, halfbeaks, needlefishes,
flying fishes y sauries fueron integrados por
Rosen (1964) en un taxon ahora conocido
como Atherinomorpha, utilizando
esencialmente caracteres osteol?gicos y
reproductivos. Revisiones posteriores han
sostenido que Atherinomorpha es un grupo
monofil?tico y han agregado otros caracteres a
la diagnosis. Hoy, los aterinomorfos est?n
definidos como monofil?ticos por
caracter?sticas derivadas del test?culo, huevos,
formas reproductoras, sistema circulatorio,
musculatura de la mand?bula, ?rgano
olfatorio, y varias partes del esqueleto,
incluyendo la regi?n etmoidea del cr?neo,
arcos branquiales, y cintura p?lvica, entre
otros. El car?cter monofil?tico de cada uno de
los tres taxa incluidos actualmente, clasificados
en los ?rdenes Cyprinodontiformes,
Beloniformes, y Atheriniformes, se define en
sus relaciones entre ellos, con variaciones de
cantidad y calidad. Durante los ?ltimos veinte
a?os, ha aumentado significativamente el uso
de datos sobre reproducci?n y moleculares
para inferir relaciones en los aterinomorfos.
En general, datos moleculares apoyan
hip?tesis basadas en la morfolog?a y, en
algunos casos, sustentan hip?tesis nuevas y
?nicas referentes a los datos morfol?gicos. Un
n?mero creciente de datos indica que todos
los aterinomorfos tienen un tipo testicular
?nico, correlacionado con una serie de
modificaciones reproductivas, tales como el
apareamiento, un periodo relativamente largo
de desarrollo, formaci?n de paquetes de
espermatozoides, fertilizaci?n interna,
superfetaci?n, retenci?n de los embriones,
diapausa, eclosi?n demorada, hermafroditismo
y viviparidad. Corroborar que alg?n grupo de
otro taxa, est? emparentado con los
aterinomorfos, puede incluir la identificaci?n
de alguno de estos aspectos del sistema
reproductor.
? Viviparous Fishes
Mari Carmen Uribe and Harry J. Grier, book editors.
New Life Publications, Homestead, Florida, 2005. p 13-30.
15
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
Introduction
In 1964, Donn E. Rosen, then curator in theDepartment of Ichthyology, American Mu-seum of Natural History, New York, pub-
lished a monograph as a Bulletin of the American
Museum of Natural History, in which he brought
together three disparate groups of teleost fishes
in one order, the Atheriniformes (Rosen, 1964).
The three suborders in Rosen?s Atheriniformes
were the Atherinoidei (the silversides, rainbow-
fishes, and phallostethids), the Cyprinodon-
toidei (the killifishes and ricefishes), and the
Exocoetoidei (the sauries, needlefishes, half-
beaks, and flying fishes). Support of this taxon
included evidence largely from two systems, os-
teology and reproductive biology, which Rosen
described in an essay, as was common then,
rather than enumerating putative synapomor-
phies. Skeletal characters that Rosen considered
diagnostic of his Atheriniformes included a disc-
shaped dorsal and ventral ossified mesethmoid
and decoupling of the rostral cartilage from the
ascending processes of the premaxillae. Repro-
ductive characters included a large, demersal egg
with long, adhesive chorionic filaments and
large oil globules (Rosen, 1964:253-255).
The new taxon, classified as the series
Atherinomorpha by Greenwood et al. (1966),
was not accepted readily by all systematic ich-
thyologists. In particular, Gosline (1971, Fig.
28B) argued that Rosen had brought together
fishes from different evolutionary grades that did
not share an evolutionary history. Atherinoids
(now classified as the order Atheriniformes fol-
lowing Dyer and Chernoff, 1996; Table 1) were
considered by Gosline to be ?higher teleosts?
because they have characters such as two dorsal
fins, both with anterior spines or thickened rays,
and an I,5 pelvic-fin ray formula. In contrast,
the Cyprinodontoidei and Exocoetoidei (Cy-
prinodontiformes and Beloniformes, following
Greenwood et al., 1966) were considered by
Gosline to be ?intermediate teleosts.? Both have
a single, soft-rayed dorsal fin and may have more
than six pelvic-fin rays, among other characters,
that they share with taxa that Gosline thought
to be less advanced (see review by Parenti, 1993).
Cyprinodontiformes and Beloniformes were not
considered closely related by Gosline (1971),
who postulated that they were derived from, or
most closely related to the Beryciformes and
Myctophiformes, respectively.
Monophyly of atherinomorphs and mono-
phyly and relationships of the three included
taxa was reviewed by Rosen and Parenti (1981)
in conjunction with a phylogenetic analysis of
Cyprinodontiformes by Parenti (1981). The
first explicitly cladistic analyses of atherino-
morph phylogeny were presented in these two
papers. Atherinomorph monophyly was sup-
ported by ten characters, again largely those of
the skeleton, but also including two reproduc-
tive characters (Rosen and Parenti, 1981:20),
one of the egg (?a large dermersal egg with long
adhesive and short filaments and many lipid
globules that coalesce at the vegetal pole?), and
one of the testis (?the spermatogonia forming
only at the blind end of the tubule near the
tunica albuginea?).
16 ? Viviparous Fishes Systematics, Biogeography, and Evolution
Table 1.
Annotated classification of Atherinomorph fishes (following Rosen and Parenti, 1981; Collette et al, 1984; Parenti, 1993;
Costa, 1998a; Dyer and Chernoff, 1996).
Series Atherinomorpha Greenwood et al., 1966 [= Atheriniformes of Rosen, 1964]
Order Atheriniformes sensu Dyer and Chernoff, 1996 [= Atherinoidei of Rosen, 1964; Division I of Rosen
and Parenti, 1981] Classification is sequenced.
Family Atherinopsidae
Suborder Atherinoidei
Family Notocheiridae (including Isonidae)
Infraorder Atherines
Family Melanotaeniidae (including Bedotiidae, Pseudomugilidae)
Family Atherionidae
Superfamily Atherinoidea
Family Phallostethidae (including Dentatherinidae)
Family Atherinidae
Superorder Cyprinodontea of Dyer and Chernoff, 1996 [Division II of Rosen and Parenti, 1981,
order Cyprinodontiformes of Nelson, 1984, not recognized by Rosen, 1964]
Order Cyprinodontiformes [= Cyprinodontoidea of Rosen, 1964]
Suborder Aplocheiloidei
Family Aplocheilidae
Family Rivulidae
Suborder Cyprinodontoidei
Superfamily Funduloidea
Family Profundulidae
Family Fundulidae
Family Goodeidae
Superfamily Valencioidea of Costa, 1998a [= Sept 1 of Parenti, 1981]
Family Valenciidae
Unranked category including superfamilies Cyprinodontoidea and Poecilioidea
Superfamily Cyprinodontoidea
Family Cyprinodontidae
Superfamily Poecilioidea of Parenti, 1981 [= unnamed clade of Costa, 1998a]
Family Anablepidae
Family Poeciliidae
Order Beloniformes [not recognized by Rosen, 1964]
Suborder Adrianichthyoidei [= Adrianichthyoidea of Rosen, 1964]
Family Adrianichthyidae (including Horaichthyidae and Oryziidae)
Suborder Exocoetoidei
Superfamily Exocoetoidea
Family Exocoetidae
Family Hemiramphidae
Superfamily Scomberesocoidea
Family Belonidae
Family Scomberesocidae
17
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
The many, unique characteristics of the
atherinomorph egg are correlated with reproduc-
tive and developmental modifications. Filaments
are derived from the secondary or outer layer of
the zona pellucida which is secreted by follicle cells
(Wourms, 1976; Wourms and Sheldon, 1976;
Loureiro and deS?, 1996). Filaments vary in
number, shape, and relative length (e.g., Able,
1984; Collette et al., 1984; White et al., 1984;
Loureiro and deS?, 1996). Oil globule number
ranges from one to over 100 (White et al., 1984:
table 93). The relatively long developmental pe-
riod in both oviparous and viviparous taxa is cor-
related with direct development, that is, loss or
reduction of a distinct larval stage, most notably
in cyprinodontiforms and beloniforms (Rosen,
1964:253).
The long developmental period and relatively
large, desiccation-resistant egg is correlated with
the evolution of delayed hatching (Martin,
1999) or diapause (Wourms, 1972). Delay of
hatching of fertilized eggs has been reported in
the atheriniform grunions of the genus Leu-
resthes, and the cyprinodontiforms Fundulus
heteroclitus, F. confluentus, and Adinia xenica
(Martin, 1999). Delay of hatching in these taxa
is facultative; fertilized, fully-developed eggs can
hatch, but are stranded in relatively dry habitats
and must await waves, tides, or rains to stimu-
late hatching (Martin, 1999; Griem and Mar-
tin, 2000). This is in contrast to fertilized eggs
of annual killifishes, which undergo diapause
and for which delay of hatching is obligatory
(Wourms, 1972). Stranding of fertilized eggs out
of water has been reported also in the Baja Cali-
fornia endemic, Fundulus lima, by Brill (1982).
Facultative delayed hatching of teleost eggs has
been reported outside atherinomorphs only in
the lower teleost osmeroid Galaxias maculatus
(Martin, 1999).
The evolutionary relationship between fac-
ultative and obligatory delay of hatching in
atherinomorphs is unknown. Phylogenetic
analyses based on molecules (e.g., Murphy and
Collier, 1997) or morphology (e.g., Costa, 1990,
1998a) have led to various, sometimes conflict-
ing, conclusions concerning single or multiple
origins of developmental diapause. A molecular
phylogenetic analysis of the family Rivulidae by
Hrbek and Larson (1999: Fig. 4) supported the
hypothesis that diapause was present in two dis-
tantly related groups of South American killi-
fishes. Rather than interpret the cladogram
literally, they considered it unlikely that diapause
had originated twice, but that presence or ab-
sence of diapause results from ?...developmen-
tal switches between alternative stabilized path-
ways? (Hrbek and Larson, 1999:1200). This was
said another way by Parenti (1981:364): ?...the
annual habit is no more than an exaggeration,
due to extreme environmental fluctuations, of a
capability of all cyprinodontiforms to survive
stress that involves desiccation?. Now, with our
increased knowledge of delayed hatching pat-
terns, I would rewrite that sentence by substitut-
ing ?atherinomorphs? for ?cyprinodontiforms?
(see also Parenti, 1993). Delayed hatching pat-
terns of atherinomorphs, whether facultative or
obligatory, may be homologous and represent
another atherinomorph synapomorphy.
The testis character proposed as an atherino-
morph synapomorphy by Rosen and Parenti
(1981) had been described just the year before
by Harry Grier and colleagues (Grier et al.,
1980; Fig. 1) who reported this distinctive tes-
tis-type in 31 atherinomorph species represent-
ing each of the three orders. Since Grier et al.
(1980), the atherinomorph testis has been re-
ported or confirmed in a total of 79 atherino-
morph species (Parenti and Grier, 2004),
including the beloniform adrianichthyid
Horaichthys setnai (Grier, 1984), seven species
of atheriniform phallostethids (Grier and
Parenti, 1994), an anablepid, Jenynsia multi-
dentata (Mart?nez and Monasterio de Gonzo,
2002), the internally-fertilizing halfbeak genus,
Zenarchopterus (Grier and Collette, 1987), and
the viviparous halfbeaks, Dermogenys, Hemi-
rhamphodon and Nomorhamphus (Downing
and Burns, 1995; Meisner and Burns, 1997a).
A possibly similar testis-type in viviparous sur-
fperches, family Embiotocidae, was noted by
Grier et al. (1980) but dismissed a year later
by Grier (1981).
Figure 1.
Diagrammatic representation of two
different testis-types in higher
teleosts: A: testis lobule in
representative atherinomorph, with
spermatogonia restricted to the
distal end of the lobule; B: testis
lobule in representative
non-atherinomorph higher teleost,
with spermatogonia distributed
throughout the length of the testis
lobule (from Grier et al., 1980: Fig. 1)
18 ? Viviparous Fishes Systematics, Biogeography, and Evolution
Evolution of viviparity is considered indepen-
dent in atherinomorphs and embiotocids (see
Lydeard, 1993). The phylogenetic significance of
reproductive characters in embiotocids, includ-
ing both egg and testis, are evaluated relative to
those of atherinomorph fishes elsewhere in this
volume (Grier et al., this volume). The derived
testis and egg are correlated in atherinomorphs
with a vast array of reproductive modifications
including coupling during mating, relatively long
developmental period, sperm-bundle formation,
internal fertilization, superfetation, embryo re-
tention, diapause, delayed hatching, hermaphro-
ditism, and live-bearing. Understanding the
phylogeny of atherinomorph fishes will be en-
hanced by an understanding of their derived re-
productive modifications and evolution of this
novel reproductive system.
The purpose of this paper is to review the
current state of our knowledge of atherino-
morph phylogeny, with a focus on live-bearing
taxa, summarizing molecular and morphologi-
cal cladistic analyses published during the past
two decades. Some phylogenetic analyses of
solely oviparous taxa are cited but not discussed
in detail. It is not my goal to summarize all
cladistic analyses of atherinomorph taxa, which
is well beyond the scope of this review.
Atherinomorph Monophyly
Atherinomorph monophyly was reviewed by
Parenti (1993) who listed 14 diagnostic charac-
ters, five of which were of reproduction and
development (Fig. 2, node A). The atherino-
morph testis-type and associated reproductive
modifications remain among the strongest evi-
dence for monophyly, as argued above.
Here, I add a fifteenth character to the athe-
rinomorph diagnosis: absence of the saccus
vasculosus, a hypothalamic circumventricular
organ of unspecified function (Tsuneki, 1992).
The saccus vasculosus has been reported to pro-
duce a parathyroid hormone-related protein in
the perciform sea bream, Sparus aurata (Devlin
et al., 1996). Approximately 200 teleost species,
both freshwater and marine, representing all ma-
jor teleost lineages, were surveyed by Tsuneki
(1992) for presence or absence of the saccus
vasculosus and extent of its development when
present. A well-developed saccus vasculosus was
considered to be a generalized condition, present
in some Osteoglossiformes, Anguilliformes, and
ostariophysans among lower teleosts, and
Mugiliformes, Gasterosteiformes, Scorpaeni-
formes, Perciformes, Pleuronectiformes, and
Tetraodontiformes among higher teleosts. The
saccus vasculosus is reduced or absent in a vari-
ety of taxa, including atherinomorphs, African
cichlids, some anabantoids, and a synbranchid
eel among higher teleosts.
The most ?clear-cut? result of this survey,
according to Tsuneki (1992:74), is that absence
of the saccus vasculosus is characteristic of
atherinomorphs, and I agree. Fifteen atherino-
morphs surveyed, representing all three orders,
from both freshwater and marine habitats un-
ambiguously lack the saccus vasculosus. Its ab-
sence is proposed here as an atherinomorph
synapomorphy.
A sixteenth atherinomorph synapomorphy,
of the oocyte, was proposed and illustrated by
Parenti and Grier (2004: Figs. 3,4). Atherino-
morph yolk is fluid, rather than granular,
throughout vitellogenesis.
Atherinomorph Sister Group
The Series Atherinomorpha was classified as sis-
ter to the Series Percomorpha by Rosen and
Parenti (1981) without an explicit proposal of
relationship to any particular percomorph ta-
xon. In diagnosing atherinomorphs, Rosen
(1964) made deliberate comparisons with taxa
such as mullets (Mugilidae) or percopsiform
fishes that had at one time been proposed as
closely related to one or another atherinomorph
order (see Parenti, 1993). In discussing ather-
inomorph sister-group relationships, Parenti
(1993: Fig. 1c) could come to no firm conclu-
sion, arguing that evidence linked atherino-
morphs to paracanthopterygians on one hand
and to percomorphs on the other.
The close relationship of mullets to ather-
inomorphs was proposed by Stiassny (1990) and
explored further by Stiassny (1993) who, al-
though she concluded that there was good evi-
dence for a sister group relationship, discussed
numerous characters that contradicted that pro-
posal. Of seven characters in support of a mul-
Figure 2.
Phylogenetic relationships among
the three orders of atherinomorph
fishes, following Rosen and Parenti
(1981), Collette et al. (1984), Parenti
(1993), Dyer and Chernoff (1996), and
this paper. Synapomorphies are: A)
testis a restricted spermatogonial
type; egg demersal, with several to
many chorionic filaments, and
several oil globules that coalesce at
the vegetal pole; coupling during
mating; prolonged developmental
period; separation of embryonic
afferent and efferent circulation by
development of heart in front of
head; ossified portion of ethmoid
region of skull highly reduced;
infraorbital series represented by
the lacrimal, dermosphenotic, and
two, one or no anterior infraorbital
bones; lateral process of pelvic bone
and distal end of pleural rib in close
association, and, in some taxa,
connected via a ligament;
supracleithrum reduced or absent;
dorsal portion of gill arches with a
large fourth epibranchial the
prominent supporting bone and no
fourth pharyngobranchial element;
medial hooklike projection and
ventral flange on the fifth
ceratobranchial bone; supraneural
bones absent; superficial division of
adductor mandibulae with two
tendons, one inserting on the
maxilla, a second inserting on the
lacrimal bone; olfactory sensory
epithelium arranged in sensory
islets; absence of the saccus
vasculosus; B) second infraorbital
bone absent; first epibranchial bone
with an expanded base and no
separate uncinate process; first
pharyngobranchial element absent;
second and third epibranchials
smaller than the first and fourth;
stomach, pyloric caecae and
pneumatic duct absent
Atheriniformes
          A
Cyprinodontiformes
                    B
Beloniformes
19
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
let-atherinomorph sister-group relationship
(Stiassny, 1993: Fig. 1), four were of the pecto-
ral girdle, two of the branchial muscles, and one
of the vertebral column. Three pelvic fin char-
acters were considered to have reversed in ather-
inomorphs (viz. Stiassny and Moore, 1992). The
study was not intended as an exhaustive review
of acanthomorph relationships, however, be-
cause, for example, another reversal in athe-
rinomorphs would be loss of transforming
ctenoid scales (Roberts, 1993).
The hypothesis of a close mullet-atherino-
morph relationship was taken a step further by
Johnson and Patterson (1993) who proposed a
new taxon, the Smegmamorpha, to include
synbranchoid eels, mastacembeloid eels, the
centrarchid Elassoma, gasterosteiforms, mullets,
and atherinomorphs. A single character was pro-
posed for smegmamorph monophyly (Johnson
and Patterson, 1993:572): the first two epineu-
ral bones originate at the tip of transverse pro-
cesses or fused parapophyses on the first two
vertebral centra. In addition, Johnson and
Patterson (1993:table 2) tabulated selected,
shared derived characters found in some, but
not all smegmamorphs, such as, for example,
infraorbital series with three or fewer bones be-
tween the lacrimal and the dermosphenotic,
present in atherinomorphs, Elassoma, gaster-
osteiforms, and synbranchoids, but absent in
mullets and mastacembeloids.
Smegmamorph monophyly was one hypo-
thesis tested by Wiley et al. (2000) in a total
evidence analysis of acanthomorph phylogeny
combining molecular and morphological data.
The strict consensus of 137 equally parsimoni-
ous trees based on morphological data recov-
ered a monophyletic Atherinomorpha with
unresolved relationships to an array of higher
taxa (Wiley et al., 2000: Fig. 8c). A strict con-
sensus of four equally parsimonious trees based
on combined molecular and morphological data
recovered a group that included the mullet
Mugil and the four atherinomorph taxa analyzed
(the atheriniforms Melanotaenia and Atherino-
morus, the beloniform Strongylura, and the
cyprinodontiform Gambusia), but did not re-
cover a monophyletic Smegmamorpha (Wiley
et al., 2000: Fig. 6). Mugil was considered to be
more closely related to the two atheriniforms
than either is to the cyprinodontiform or the
beloniform; that is, atherinomorph monophyly
was refuted as well. Morphological characters
surveyed by Wiley et al. (2000), however, did
not include characters such as the atherino-
morph testis-type (not found in mullets; Grier
et al., 1980), absence of the saccus vasculosus
(well-developed in mullets; Tsuneki, 1992), or
innervation of the pectoral and pelvic fin
muscles by branches of spinal nerve 2 (present
and derived in mullets, absent in atherino-
morphs; Parenti and Song, 1996). Detailed
molecular analyses of acanthomorph phylogeny
based on molecular data alone (e.g., Miya et al.,
2003) confirm atherinomorph monophyly, but
include other taxa, such as blennioids and go-
biesocids, along with mullets, as putative ather-
inomorph sister taxa. Broader surveys of
morphology, as well as molecules, are needed to
further test monophyly of smegmamorphs and
evaluate the hypothesis of a sister group rela-
tionship of mullets and atherinomorphs.
Cyprinodontea
Relationships among the three groups of ather-
inomorph fishes were unspecified by Rosen
(1964). Monophyly of each group and the rela-
tionships among them were considered by Rosen
and Parenti (1981:21-23) who proposed a sister
group relationship between Cyprinodontiformes
and Beloniformes, together called Division II
atherinomorphs. Four characters were proposed
to support monophyly of Division II (Rosen and
Parenti, 1981:21; Fig. 2, node B). A fifth charac-
ter may be added from Li (2001:585): absence of
a stomach, including absence of pyloric caecae
and a pneumatic duct.
The sister group relationship between
Cyprinodontiformes and Beloniformes has been
corroborated (Stiassny, 1990; Saeed et al., 1994;
Dyer and Chernoff, 1996; Wiley et al., 2000;
Li, 2001). The relationship was recognized by
Nelson (1984:214) who in his second edition
of Fishes of the World synonymized the two or-
ders in an expanded Cyprinodontiformes. This
decision was reversed in the third edition
(Nelson, 1994:264, with the three orders Ather-
iniformes, Beloniformes, and Cyprinodonti-
formes recognized without inter-ordinal
relationships expressed). The current edition of
Fishes of the World is used worldwide as a stan-
dard reference for teleost classification, however,
and an enlarged order Cyprinodontiformes, in-
cluding beloniforms, was incorporated into nu-
merous publications, particularly during the
decade between 1984 and 1994 (e.g., Tsuneki,
1992; Kottelat et al., 1993). The superorder
Cyprinodontea was proposed by Dyer and
Chernoff (1996) as a formal name for Rosen
20 ? Viviparous Fishes Systematics, Biogeography, and Evolution
and Parenti?s (1981) Division II, the Cyprino-
dontiformes and Beloniformes, and is adopted
here (Table 1).
Cyprinodontiformes
The first explicitly cladistic analysis of cypri-
nodontiform fishes was based largely on os-
teological characters (Parenti, 1981; Fig. 3).
Cyprinodontiform monophyly was corroborated
by six complex characters (Parenti, 1981: Fig. 9,
node a), and it has been challenged only by Li
(2001; see comments below under Beloniformes).
One cyprinodontiform character of Parenti
(1981), prolonged embryonic development, is
discussed above as an atherinomorph synapo-
morphy (see also Parenti, 1993). A major conclu-
sion of Parenti?s (1981) study that refuted earlier
notions of cyprinodontiform relationships was
that viviparity had evolved at least three times
within the order, not once. That is, oviparous sis-
ter groups of each group of viviparous taxa were
hypothesized. Also, cyprinodontiforms were di-
vided into two monophyletic suborders, the
Aplocheiloidei and Cyprinodontoidei. This pro-
posal of relationships was tested by Meyer and
Lydeard (1993; Fig. 4) using partial DNA se-
quences of the tyrosine kinase gene X-src, an
oncogene chosen in part because cyprinodonti-
forms of the genus Xiphophorus have long been
known to inherit melanomas (see Schartl, 1995).
No non-cyprinodontiform taxon was used as an
outgroup by Meyer and Lydeard, so their analysis
was not a test of cyprinodontiform monophyly.
Also, at least one pivotal taxon, the oviparous
Oxyzygonectes, sister to the viviparous Anableps
and Jenynsia in the Anablepidae, according to
Parenti (1981), was not included. Nonetheless,
the maximum parsimony phylogenetic hypoth-
esis of Meyer and Lydeard (1993) corroborated
Parenti?s (1981) conclusions that viviparity had
evolved at least three times within cyprinodonti-
forms, in anablepids, goodeids, and poeciliids.
Further, the analysis recovered the controversial
sister group relationship of the viviparous good-
eids and their oviparous relatives, Empetrichthys
and Crenichthys (see also Grant and Riddle, 1995).
Cyprinodontiforms were used as a test taxon
by Parker (1997) to evaluate the consequences
of combining morphological and molecular data
in a phylogenetic analysis. Morphological char-
acters described by Parenti (1981, 1984a) are
listed and character states coded in a detailed
appendix (Parker, 1997:184-185). Although this
study was not intended as a thorough re-analy-
Figure 3.
Phylogenetic relationships among
families of Cyprinodontiformes as
proposed by Parenti (1981)
Figure 4.
Phylogenetic relationships among
select genera of Cyprinodontiformes
as proposed by Meyer and Lydeard
(1993) based on partial DNA
sequences of the tyrosine kinase
gene X-src. Genera in boxes
represent families or subfamily
groupings of live-bearing taxa and
their close relatives, as also
proposed by Parenti (1981), from top
to bottom, family Goodeidae, family
Anablepidae, and subfamily
Poeciliinae
Aplocheilidae
Rivulidae
Profundulidae
Fundulidae
Valenciidae
Anablepidae
Poeciliidae
Goodeidae
Cyprinodontidae
Nothobranchius
Cynolebias
Rivulus
Rivulus
Fundulus
Crenichthys
Zoogoneticus
Zoogoneticus
Xenotoca
Profundulus
Anableps
Jenynsia
Cnesterodon
Poecilia
Xiphophorus
Xiphophorus
Tomeurus
Aplocheilichthys
Aplocheilichthys
Fluviphylax
Cubanichthys
Cyprinodon
Jordanella
21
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
sis of Parenti?s (1981) hypothesis, some of
Parker?s results anticipated those of other stud-
ies. For example, Tomeurus, the ovoviviparous
poeciliine, had been considered primitive to vi-
viparous poeciliines since Rosen and Bailey?s
(1963) classic review, and this relationship was
corroborated by Meyer and Lydeard (1993; Fig.
4). In contrast, a partitioned X-src dataset of first
and second codon positions only, analyzed un-
der maximum parsimony (Parker, 1997: Fig. 2),
supported the sister group relationship of To-
meurus and Cnesterodon, a viviparous poeciliine,
together considered derived, not basal, poeci-
liines. This relationship was corroborated by an
array of synapomorphies in a parsimony analy-
sis of morphological characters by Ghedotti
(2000; Fig. 5), including neural arch of first ver-
tebra open dorsally, lateral processes on ventral
portion of seventh, eighth, and ninth proximal
anal-fin radials in adult males present and in
contact, and distal tip of the gonopodium with
elongate, bony processes. These morphological
characters were of course known to Rosen and
Bailey (1963) who likely accepted the constraint
that an ovoviviparous taxon such as Tomeurus
was basal to a group of viviparous taxa. This
constraint was relaxed by Parker (1997) and
Ghedotti (2000) who independently recovered
a novel hypothesis of relationships of Tomeurus.
Division of Cyprinodontiformes into two sub-
orders, Aplocheiloidei and Cyprinodontoidei,
was corroborated by Costa (1998a; Fig. 6) who
re-analyzed killifish phylogenetic relationships
using morphology. The hypothesis of Costa
(1998a; Fig. 6) differs from that of Parenti (1981;
Fig. 3) in the placement of Goodeidae as sister to
Profundulidae, not Cyprinodontidae, and the
resolution of the relationships of Valenciidae.
Both studies used osteology as a principal source
of data, but differed in interpretation of signifi-
cance of character states of the premaxilla, among
others. The sister group relationship of Good-
eidae and Profundulidae was recovered also in the
molecular hypotheses of Meyer and Lydeard
(1993) and Parker (1997). The close relationships
of fundulids, goodeids, and profundulids is re-
flected in the written classification of Cyprin-
odontiformes (Table 1).
Monophyly of each of the nine families rec-
ognized by Parenti (1981) was corroborated by
Costa (1998a) and the terminal taxa of Meyer
and Lydeard?s (1993; Fig. 4) hypothesis are also
consistent with Parenti?s hypothesis. Monophyly
of the Anablepidae and Poeciliidae (sensu
Parenti, 1981) was corroborated in Ghedotti?s
Figure 5.
Phylogenetic relationships among
the poecilioid fishes, simplified from
Ghedotti (2000: Fig. 20). Species
listed are members of the subfamily
Poeciliinae
Figure 6.
Phylogenetic relationships among
families of Cyprinodontiformes as
proposed by Costa (1998a)
Anablepidae
Aplocheilichthyinae
Procatopodinae
Alfaro cultratus
Priapella compressa
Gambusia affinis
Heterandria formosa
Poeciliopsis latidens
Girardinus metallicus
Poecilia sphenops
Phallichthys amates
Phallotorynus victoriae
Phalloceros caudimaculatus
Cnesterodon decemmaculatus
Tomeurus gracilis
Aplocheilidae
Rivulidae
Profundulidae
Goodeidae
Fundulidae
Valenciidae
Anablepidae
Poeciliidae
Cyprinodontidae
22 ? Viviparous Fishes Systematics, Biogeography, and Evolution
(2000; Fig. 5) morphological analysis, whereas
Meyer and Lydeards? (1993; Fig. 4) analysis pro-
posed a paraphyletic Poeciliidae. The dotted
lines in Meyer and Lydeard?s (1993; Fig. 4) cla-
dogram indicate relationships for which they
found weak support, however. Morphology and
molecules do equally well, i.e. agree, in resolv-
ing relationships at the tips of the tree, but vary
in their ability to recover higher taxa. A mo-
lecular phylogenetic analysis of aplocheiloids by
Murphy and Collier (1997) conflicts, in part,
with the proposals of Parenti (1981) and Costa
(1998a) based on morphology. A stable classifi-
cation of cyprinodontiforms, at the family level
and above, is within reach, however, and is ex-
pected to include components common to the
above morphological and molecular analyses.
Additional molecular phylogenies of families
or other subgroups of aplocheiloids include
those of Murphy and Collier (1999, Aphyo-
semion and Fundulopanchax), Murphy et al.
(1999a, West African aplocheiloids), and
Murphy et al. (1999b, Rivulidae). Morphologi-
cal phylogenies or surveys include Costa (1990,
1998b, Rivulidae; 1995a, Cynopoecilus; 1995b,
Cynolebiatinae; 1996a, Simpsonichthys),
Loureiro and deS? (1998, Cynolebias), and Aarn
and Shepherd (2001, epiplatines). Taxonomy,
biology, and conservation status of Brazilian
annual killifishes was reviewed by Costa (2002,
and references therein).
Molecular phylogenies of families or other
subgroups of cyprinodontoids include Bernardi
(1997, Fundulidae), Breden et al. (1999, Poeci-
lia), Grady et al. (2001, Fundulus), Hamilton
(2001, Limia), Hrbek and Meyer, 2003 (Apha-
nius) L?ssen et al. (2003, Orestias), Lydeard et
al. (1995, Gambusia), Mojica et al. (1997,
Brachyrhaphis), Parker and Kornfield (1995,
cyprinodontids), and Webb et al. (2004,
livebearing Goodeidae). Morphological phylo-
genies or surveys include Parenti (1984a, Ores-
tias), Chambers (1987, cyprinodontiform
gonopodia; 1990, cnesterodontin gonopodia),
Ghedotti (1998, Anablepidae), Rauchenberger
(1989, Gambusia), Costa (1996b, Fluviphylax;
1997, cyprinodontids), and Rodr?guez (1997,
Poeciliini). Conclusions of these studies that
bear on higher order relationships of cyprin-
odontiforms were summarized by Lazara
(2001:ix-xiv).
The genus Xiphophorus, the swordtails and
platyfishes, serves as a model taxon in analyses
of congruence of phylogenetic pattern with be-
havior, development, morphology, and mol-
ecules (see, for example, Basolo, 1991; Haas,
1993; Meyer et al., 1994, Marcus and McCune,
1999, and Morris et al., 2001).
Beloniformes
Beloniform monophyly was supported by seven
synapomorphies (Rosen and Parenti, 1981:17),
including absence of the interhyal bone, reduc-
tion or loss of the interarcual cartilage, presence
of only a single, ventral hypohyal bone, modifi-
cations of the gill arch skeleton, as well as a dis-
tinctive caudal skeleton characterized by the
lower caudal lobe with more principal rays than
in the upper caudal lobe.
Beloniform relationships were reviewed by
Collette et al. (1984; Fig. 7) who accepted a
monophyletic Beloniformes including Rosen
and Parenti?s (1981) proposal that ricefishes
(family Adrianichthyidae) are more closely re-
lated to exocoetoids (families Exocoetidae,
Hemiramphidae, Belonidae, and Scomberesoci-
dae) than to cyprinodontiforms. This proposal
has been criticized recently by Li (2001) who
argued that adrianichthyoids are more closely
related to Cyprinodontiformes than to exo-
coetoids. In particular, Li (2001) claimed that
some characters proposed as diagnostic of
Beloniformes sensu lato, although absent in the
primitive cyprinodontiform suborder Aplochei-
loidei, are present in the derived suborder
Cyprinodontoidei. For example, Li (2001:584)
rejected Rosen and Parenti?s (1981) beloniform
synapomorphy of a single, ventral hypohyal be-
cause cyprinodontoids have a single hypohyal.
If we accept cyprinodontiform monophyly,
however, which is supported by a symmetrical
caudal fin skeleton, absent in adrianichthyoids,
and first pleural rib on the second, rather than
Adrianichthyidae
Exocoetidae
Hemiramphidae
Belonidae
Scomberesocidae
Figure 7.
Phylogenetic relationships among
the families of beloniform fishes,
following Rosen and Parenti (1981)
and Collette et al. (1984)
23
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
the third vertebra, among other characters, then
similarities between cyprinodontoids and
adrianichthyoids must be interpreted as conver-
gent rather than indicative of close relationship.
Cyprinodontiforms and beloniforms, sensu
Rosen and Parenti (1981), are readily distin-
guished by their distinct caudal fin skeletons.
Finally, both cyprinodontiforms and adrianich-
thyoids were characterized by Li (2001) as lack-
ing elongate jaws, whereas Parenti (1987,
1989a) argued that the elongate jaws of the
large-bodied adrianichthyoids of Sulawesi, some
of which have been called ?duck-billed? repre-
sent additional support for their close relation-
ship to exocoetoids. Despite rejection of Li?s
(2001) hypothesis, I appreciate his comments
as they call for continued critique of the mono-
phyly of clades within the Atherinomorpha as
recognized herein.
Higher-order beloniform sensu lato relation-
ships were reviewed by Lovejoy (2000; Fig. 8)
who combined data from nuclear and mito-
chondrial gene sequences with morphology in a
total evidence analysis. The families Exocoetidae
(flyingfishes) and Scomberesocidae (sauries)
were considered monophyletic by both Collette
et al. (1984; Fig. 7) and Lovejoy (2000; Fig. 8).
The families Hemiramphidae (halfbeaks) and
Belonidae (needlefishes), considered monophyl-
etic by Collette et al. (1984), were hypothesized
to be paraphyletic by Lovejoy (2000).
No non-beloniform taxon was included in
Lovejoy?s analysis and a single adrianichthyid spe-
cies (Oryzias matanensis) was an outgroup to the
ingroup exocoetoids. Therefore, the analysis was
not a test of beloniform or of exocoetoid mono-
phyly. Further, some intriguing taxa were not in-
cluded in the study, such as the southern African
needlefish, Petalichthys, which remains in a
?halfbeak stage? of development for a relatively
long time before both upper and lower jaws be-
come elongate (Collette et al., 1984:342;
Boughton et al., 1991). Also missing was the
hemiramphid Oxyporhamphus recently reclassi-
fied as a flyingfish, family Exocoetidae, based on
a re-analysis of morphology (Dasilao et al., 1997).
Nonetheless, Lovejoy?s (2000; Fig. 8) hypothesis
offers a novel reinterpretation of traditional
beloniform morphology and invites further study
of the relationship between morphological and
molecular data as used in phylogenetic analyses.
Molecular sequences and morphology were com-
bined in a total evidence analysis of phylogenetic
relationships of New World needlefishes by
Lovejoy and Collette (2001).
Monophyly of the internally-fertilizing
halfbeaks, genera Zenarchopterus, Hemirham-
phodon, Dermogenys, and Nomorhamphus, was
supported by the morphological studies of Ander-
son and Collette (1991), Downing and Burns
(1995), Meisner and Burns (1997b), Meisner and
Collette (1999), and Meisner (2001). Petalichthys
and Oxyporhamphus were included in a reanaly-
sis of beloniform phylogeny by Lovejoy et al.
(2004) and paraphyly of hemiramphids and
belonids corroborated. The last three halfbeak
genera are viviparous and together form a mono-
phyletic group as corroborated by these analyses.
A fifth genus, the monotypic Tondanichthys, de-
scribed from the type series of ten specimens that
does not include a mature male, is inferred to be
internally fertilizing (Collette, 1995; Meisner and
Collette, 1999).
Reproductive biology has been used to infer
phylogenetic relationships among live-bearing
halfbeaks. Dermogenys is diagnosed by large
sperm bundles and intrafollicular development;
whereas, Nomorhamphus is diagnosed by small
sperm bundles and a long intraluminal devel-
opmental period (Downing and Burns, 1995;
Meisner and Burns, 1997b; Meisner and
Collette, 1999; Meisner, 2001). These generic
limits are in contrast to those of Brembach
(1991).
Ricefish females are known to carry bundles
of fertilized eggs until hatching (Fig. 9), rather
than depositing them on over-hanging vegeta-
tion or the substrate. Aquarium-maintained O.
Figure 8.
Phylogenetic relationships among
beloniform fishes, simplified from
Lovejoy (2000: Fig. 2). The families
Exocoetidae and Scomberesocidae
were each considered
monophyletic; the families
Hemiramphidae and Belonidae
paraphyletic. ?Hemiramphids (IF)?
refers to the four internally fertilizing
genera, Zenarchopterus,
Nomorhamphus, Dermogenys and
Hemirhamphodon
Oryzias matanensis
Exocoetidae
hemiramphids
hemiramphids
hemiramphids (IF)
belonids
belonids
belonids
belonids
Scomberesocidae
24 ? Viviparous Fishes Systematics, Biogeography, and Evolution
nigrimas females reportedly carry large bundles
of eggs, but deposit them among plants or on
the substrate soon after spawning (Kottelat,
1990a:54). In spawning in open water, ricefishes
are similar to the above mentioned Fundulus
lima (Brill, 1982). Embryos in the clusters are
relatively well developed, with large, well-
formed eyes and pigmented bodies, and appear
near hatching (Fig. 10). Because these fertilized
eggs may be carried until hatching, Kottelat
(1990a:62) proposed that ricefishes be consid-
ered a distinct reproductive guild for which he
coined the term ?pelvic brooders.? This repre-
sents one of the few cases of parental care in
oviparous atherinomorphs. Females carrying
clusters of fertilized eggs, long known in the
medaka, Oryzias latipes (Yamamoto, 1975:7),
has been reported in at least eight other ricefish
species, O. dancena (Fig. 9), O. nigrimas (Kot-
telat, 1990a:54) X. oophorus (Kottelat, 1990a:
Fig. 6), X. sarasinorum (Fig. 10), O. marmoratus
(Kottelat, 1990b: Fig. 5), O. matanensis (Kotte-
lat, 1990b:161), O. javanicus (BMNH 1970.
7.22:38-39), O. luzonensis (Blanco, 1947) and
is likely to occur in others.
The Indian ricefish, Horaichthys setnai, is in-
ternally fertilizing and lays fertilized eggs
(Kulkarni, 1940). Internal fertilization and em-
bryo retention is facultative in some ricefishes.
Facultative embryo retention was reported in the
medaka, Oryzias latipes, by Amemiya and
Murayama (1931). One specimen of Adrianich-
thys kruyti, a large, pelagic ricefish from Lake
Poso, Sulawesi, was reported to be hermaphro-
ditic, having both testis and ovary, by Klie
(1988, in Kottelat, 1990a:57). Much informa-
tion available on the reproduction of the large
Figure 9.
Oryzias dancena, USNM 313908,
female, 23.8 mm SL, with cluster of
fertilized eggs. Photo by H. H. Tan
Figure 10.
Xenopoecilus sarasinorum, CMK
6557, female, 53.4 mm SL. Above,
embryo cluster held to body
posterior to pelvic fins. Below, same
specimen, chorion measures
approximately 2 mm in diameter Fig. 9
Fig. 10
25
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
ricefishes is anecdotal (see Weber and de Beau-
fort, 1922; Kottelat, 1990a; Rosen, 1964). More
detailed study of the reproductive morphology
of the large Sulawesi ricefishes is needed to de-
termine the extent of internal fertilization, em-
bryo retention, and hermaphroditism in the
Adrianichthyidae.
Atheriniformes
Since 1981, there have been several, solely mor-
phological, phylogenetic analyses of atherini-
form fishes (White et al., 1984; Stiassny, 1990;
Saeed et al., 1994; and Dyer and Chernoff,
1996; Fig. 11). Monophyly of atheriniforms was
not supported by Rosen and Parenti (1981) or
Parenti (1984b), but it has been argued for
strongly in these other studies.
Atheriniform monophyly was supported by
two developmental characters by White et al.
(1984:357): short preanal length of flexion lar-
vae and a single row of melanophores on the
dorsal margin of larvae. Eight adult characters
were added to the diagnosis by Dyer and
Chernoff (1996:1): vomerine ventral face con-
cave, long A1 muscle tendon to lacrimal, two
anterior infraorbital bones, pelvic-rib ligament,
pelvic medial plate not extended to anterior end,
and second dorsal-fin spine flexible.
This atheriniform diagnosis requires ho-
moplasy within several characters. For example,
newly hatched adrianichthyids also have a single
row of dorsal melanophores (White et al.,
1984:359). Number of anterior infraorbital bones
ranges from one to three in atheriniforms (Dyer
and Chernoff, 1996). The three anterior infraor-
bital bones of the rainbowfishes Melanotaenia and
Chilatherina were considered evidence of their
sister-group relationship by Dyer and Chernoff
(1996:67), whereas Rosen and Parenti (1981)
considered the character to be primitive for
atherinomorphs. Outgroups of atheriniforms in
Dyer and Chernoff ?s (1996: Table 2) data matrix
include representative cyprinodontiform and
beloniform taxa and the mullet, Mugil. Given the
strong support for atherinomorph monophyly
and the tentative support for a mullet-ather-
inomorph sister group relationship, as argued
above, additional acanthomorph outgroups may
yield alternate interpretations of phylogeny when
included in a parsimony analysis of either mor-
phological or molecular data.
Despite the ambiguity in distribution of char-
acters discussed above, I use the formal term
order Atheriniformes for the included taxa be-
cause it is more popular than the vernacular
?atherinoids.?
Phylogenetic analyses of atheriniform sub-
groups include an analysis of the internally
fertilizing freshwater and coastal family Phal-
lostethidae, proposed as sister taxon of the ma-
rine Dentatherina (Parenti, 1984b, 1989b). This
sister group relationship was corroborated by
Dyer and Chernoff (1996) who classified
Dentatherina in an expanded Phallostethidae.
Atheriniformes are oviparous, although report
of facultative embryo retention would not be
surprising. Phallostethids (sensu Parenti, 1989b)
are internally fertilizing and lay fertilized eggs.
Internal fertilization was reported in the brook
silverside, Labidesthes sicculus, by Grier et al.
(1990).
Other morphological phylogenies of sub-
groups of Atheriniformes include Chernoff
(1986, menidiines), Saeed et al. (1989, Pseudo-
mugilidae), and Dyer (1998, Atherinopsidae).
Conclusions
The series Atherinomorpha is a well-corrobo-
rated, monophyletic taxon. As for other such
well-corroborated taxa, the list of characters
diagnostic of the Atherinomorpha continues to
grow (Rosen and Parenti, 1981; Parenti, 1993;
Figure 11.
Phylogenetic relationships among
the subfamilies, families or tribes of
atheriniform fishes as proposed by
Dyer and Chernoff (1996), following
Dyer (1998: Fig. 1d)
Atherinopsidae
Notocheiridae
Bedotiinae
Melanotaeniinae
Telmatherinini
Pseudomugilini
Atherionidae
Dentatherininae
Phallostethinae
Atherinomorinae
Craterocephalinae
Atherininae
26 ? Viviparous Fishes Systematics, Biogeography, and Evolution
herein). Each of its included orders, the Cyprin-
odontiformes, Beloniformes, and Atherini-
formes is monophyletic, although the quality
and quantity of support for each is variable.
Molecular tests of morphological hypotheses
of atherinomorph relationships agree, in large
part. Where they differ, molecules present novel
hypotheses of relationship, most notably in
beloniforms (Lovejoy, 2000), and invite rein-
terpretations of our traditional understanding
of morphological characters. Not all molecular
analyses agree, however. Two phylogenetic hy-
potheses based on partial sequences of the
oncogene, X-src, yielded different interpretations
of relationships of the poeciliid Tomeurus. No-
tably, Parker?s (1997: Fig. 2) hypothesis of the
sister group relationship of Tomeurus and
Cnesterodon was corroborated in a reinterpreta-
tion of morphological data by Ghedotti (2000).
Molecular and morphological hypotheses may
inform each other and point to weak areas in
the other analysis. The Cyprinodontiformes has
been studied most intensively during the past
twenty years; morphological and molecular
analyses share repeated statements of relation-
ship to such a degree that a stable classification
of the order is within reach.
Monophyly of the order Atheriniformes has
been supported by numerous morphological
studies, most recently that of Dyer and Chernoff
(1996). Interpretation of polarity of the charac-
ters used by Dyer and Chernoff (1996) to diag-
nose atheriniforms hinges on the choice of an
atherinomorph outgroup, however. Their choice
of mullets may be appropriate, but a broader
range of outgroup taxa may yield other interpre-
tations of atheriniform relationships. A molecu-
lar test of the Dyer and Chernoff (1996)
hypothesis may reveal novel relationships as well.
As for cyprinodontiforms and beloniforms, how-
ever, a molecular hypothesis of atheriniforms will
not substitute for that based on morphology.
Atherinomorph fishes likely will continue to
be studied broadly, especially as they include nu-
merous model organisms, such as the poeciliids
Xiphophorus, Poecilia, and Gambusia, the
ricefishes Oryzias, as well as a wide range of live-
bearing teleost fish taxa in the families Goodeidae
and Anablepidae and other poeciliids. Phyloge-
netic hypotheses of atherinomorphs and their
subgroups are among the most examined and
re-examined within bony fishes, which makes
their continued use as model organisms and their
unique role in understanding evolution of fish
reproduction even more justifiable.
Acknowledgments and abbreviations
I am indebted to the organizers, Mari Carmen
Uribe, Ra?l Pineda, Topiltzin Contreras and
Harry J. Grier for inviting me to participate in
the II International Symposium on Livebearing
Fishes. Research on ricefish systematics was sup-
ported, in part, by NSF grant BSR 87-00351.
Heok Hui Tan, National University of Singa-
pore, photographed the ricefish in figure 8.
Maurice Kottelat, Switzerland, lent specimens in
his care and discussed ricefish systematics. Dar-
rell Siebert allowed access to specimens at the
BMNH. My colleagues, Ralf Britz, Bruce Col-
lette, Carlos Figueiredo, Dave Johnson, Amy
Meisner, Joe Nelson, and Melanie Stiassny read
and provided helpful comments on earlier ver-
sions of the manuscript.
Institutional abbreviations: BMNH, The
Natural History Museum, London; USNM,
United States National Museum of Natural His-
tory, Washington, DC; CMK, Collection of
Maurice Kottelat, Cornol, Switzerland.
27
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System
References
Aarn, Shepherd AM. 2001. Descriptive anatomy of
Epiplatys sexfasciatus (Cyprinodontiformes: Aplocheili-
dae) and a phylogenetic analysis of Epiplatina. Cy-
bium 25:209-225.
Able KW. 1984. Cyprinodontiformes: development. In:
Moser HG, Richards WJ, Cohen DM, Fahay MP,
Kendall AW, Jr., Richardson SL, editors, Ontogeny
and systematics of fishes. Special Publication No. 1
Supplement to Copeia. American Society of Ichthy-
ologists and Herpetologists. p 362-368.
Amemiya I, Murayama S. 1931. Some remarks on the
existence of developing embryos in the body of an
oviparous cyprinodont, Oryzias (Aplocheilus) latipes
(Temminck and Schlegel). Proc Imp Acad Japan
7:176-178.
Anderson WD III, Collette BB. 1991. Revision of the
freshwater viviparous halfbeaks of the genus Hemir-
hamphodon (Teleostei: Hemiramphidae). Ichthyol
Explor Freshwaters 2:151-176.
Basolo AL. 1991. Male swords and female preferences.
Science 253:1426-1427.
Bernardi G. 1997. Molecular phylogeny of the Funduli-
dae (Teleostei, Cyprinodontiformes) based on the cy-
tochrome b gene. In: Molecular Systematics of Fishes.
Kocher TD, Stepien CA, editors, Academic Press, San
Diego. p 189-197.
Blanco GJ. 1947. The breeding activities and embryology
of Aplocheilus luzonensis Herre and Ablan. Philippine
J Sci 77:89-93.
Boughton DA, Collette BB, McCune AR. 1991. Hetero-
chrony in jaw morphology of needlefishes (Teleostei:
Belonidae). Syst Zool 40:329-354.
Breden F, Ptacek MB, Rashed M, Taphorn D, Figueiredo
CA. 1999. Molecular phylogeny of the live-bearing
fish genus Poecilia. Mol Phyl Evol 12:95-104.
Brembach M. 1991. Systematik und Fortplflanzungsbiologie
der lebendb?renden Halbschn?bler der gattung Der-
mogenys und Nomorhamphus (Hemirhamphidae [sic],
Pisces). Verlag Natur Wissenschaft Solingen. 201 pages.
Brill, JS, Jr. 1982. Observations on the unique reproduc-
tive behavior of Fundulus lima Vaillant a killifish from
Baja, [sic] California. Freshwater Mar Aquar 5:9-10,
12-15, 74-76, 78, 79, 82, 84-87, 90.
Chambers J. 1987. The cyprinodontiform gonopodium,
with an atlas of the gonopodia of the fishes of the ge-
nus Limia. J Fish Biol 30:389-418.
Chambers J. 1990. The gonopodia of the fishes of the
tribe Cnesterodontini (Cyprinodontiformes, Poeci-
liidae). J Fish Biol 36:903-916.
Chernoff B. 1986. Phylogenetic relationships and reclas-
sification of menidiine silverside fishes with emphasis
on the tribe Membradini. Proc Acad Nat Sci Phila
138(1):189-249.
Collette BB. 1995. Tondanichthys kottelati, a new genus
and species of freshwater halfbeak (Teleostei: Hemir-
amphidae) from Sulawesi. Ichthyol Explor Freshwa-
ters 6:171-174.
Collette BB, McGowen GE, Parin NV, Mito S. 1984.
Beloniformes: development and relationships. In:
Moser HG, Richards WJ, Cohen DM, Fahay MP,
Kendall AW, Jr., Richardson SL. editors, Ontogeny
and systematics of fishes. Special Publication No. 1,
Supplement to Copeia. American Society of Ichthy-
ologists and Herpetologists. p 335-354.
Costa WJEM. 1990. An?lise filogen?tica da fam?lia
Rivulidae (Cyprinodontiformes, Aplocheiloidei). Rev
Brasil Biol 50:65-82.
Costa WJEM. 1995a. Revision of the neotropical annual
fish genus Cynopoecilus (Cyprinodontiformes: Rivuli-
dae). Copeia. 1995:456-465.
Costa WJEM. 1995b. Pearl Killifishes, the Cynolebia-
tinae, systematics and biogeography of the neotropical
annual fish subfamily (Cyprinodontiformes: Rivuli-
dae). TFH Publications, Inc. Neptune City, NJ.
Costa WJEM. 1996a. Phylogenetic and biogeographic
analysis of the neotropical annual fish genus Simpson-
ichthys (Cyprinodontiformes: Rivulidae). J Comp Biol
1:129-140.
Costa WJEM. 1996b. Relationships, monophyly and
three new species of the neotropical miniature poeci-
liid genus Fluviphylax (Cyprinodontiformes: Cyprin-
odontoidei). Ichthyol Explor Freshwaters 7:111-130.
Costa WJEM. 1997. Phylogeny and classification of the
Cyprinodontidae revisited (Teleostei: Cyprinodonti-
formes): Are Andean and Anatolian killifishes sister
taxa? J Comp Biol 2:1-17.
Costa WJEM. 1998a. Phylogeny and classification of the
Cyprinodontiformes (Euteleostei: Atherinomorpha) a
reappraisal. In: Malabarba LR, Reis RE, Vari RP,
Lucena ZMS, Lucena CAS, editors, Phylogeny and
Classification of Neotropical Fishes, EDIPUCRS
(Editora Pontif?cia Universidade Cat?lica do Rio
Grande do Sul), Porto Alegre, Brazil. p 537-560.
Costa WJEM. 1998b. Phylogeny and classification of
Rivulidae revisited: origin and evolution of annualism
and miniaturization in rivulid fishes (Cyprinodonti-
formes: Aplocheiloidei). J Comp Biol 3:33-92.
Costa WJEM. 2002. Peixes Anuais Brasileiros. Diversi-
dade e Conserva??o. S?rie Pesquisa no. 60. Editora da
UFPR, Curitiba.
Dasilao JC Jr, Sasaki K, Okamura O. 1997. The hemir-
amphid Oxyporhamphus is a flyingfish (Exocoetidae).
Ichthyol Res 44:101-107.
Devlin AJ, Danks JA, Faulkner MK, Power DM, Canario
AVM, Martin TJ, Ingleton PM. 1996. Immuno-
chemical detection of a parathyroid hormone-related
protein in the saccus vasculosus of a teleost fish. Gen
Comp Endocrin 101:83-90.
Downing AL, Burns JR. 1995. Testis morphology and
spermatozeugma formation in three genera of vivipa-
rous halfbeaks: Nomorhamphus, Dermogenys, and
Hemirhamphodon. J Morph 225:329-343.
Dyer BS. 1998. Phylogenetic systematics and historical
biogeography of the neotropical silverside family
Atherinopsidae (Teleostei: Atheriniformes). In: Mala-
barba LR, Reis RE, Vari RP, Lucena ZMS, Lucena
CAS, editors, Phylogeny and classification of Neotro-
pical Fishes, EDIPUCRS (Editora Pontif?cia Univer-
sidade Cat?lica do Rio Grande do Sul), Porto Alegre,
Brazil. p 519-536.
Dyer BS, Chernoff B. 1996. Phylogenetic relationships
among atheriniform fishes (Teleostei: Atherinomor-
pha). Zool J Linn Soc 117:1-69.
Ghedotti MJ. 1998. Phylogeny and classification of the
Anablepidae (Teleostei: Cyprinodontiformes). In:
Malabarba LR, Reis RE, Vari RP, Lucena ZMS,
Lucena CAS, editors, Phylogeny and classification of
Neotropical Fishes, EDIPUCRS (Editora Pontif?cia
Universidade Cat?lica do Rio Grande do Sul), Porto
Alegre, Brazil. p 561-582.
Ghedotti MJ. 2000. Phylogenetic analysis and taxonomy
of the poecilioid fishes (Teleostei: Cyprinodonti-
formes). Zool J Linn Soc 130:1-53.
Gosline WA. 1971. Functional Morphology and classifi-
cation of teleostean fishes. The University of Hawaii
Press, Honolulu.
Grady JM, Coykendall DK, Collette BB, Quattro JM.
2001. Taxonomic diversity, origin, and conservation sta-
tus of Bermuda killifishes (Fundulus) based on mitochon-
drial cytochrome b phylogenies. Conserv Gen 2:41-52.
Grant EC, Riddle BR. 1995. Are the endangered spring-
fish (Crenichthys Hubbs) and poolfish (Empetrichthys
Gilbert) fundulines or goodeids? A mitochondrial
DNA assessment. Copeia 1995:209-212.
Greenwood PH, Rosen DE, Weitzman SH, Myers GS.
1966. Phyletic studies of teleostean fishes, with a pro-
visional classification of living forms. Bull Amer Mus
Nat Hist 131:345-455.
Griem JN, Martin KLM. 2000. Wave action: the environ-
mental trigger for hatching in the California grunion
Leuresthes tenuis (Teleostei: Atherinopsidae). Mar Biol
137:177-181.
Grier HJ. 1981. Cellular organization of the testis and
spermatogenesis in fishes. Amer Zool 21:345-357.
Grier HJ. 1984. Testis structure and formation of sper-
matophores in the atherinomorph teleost Horaichthys
setnai. Copeia 1984:833-839.
Grier HJ, Collette BB. 1987. Unique spermatozeugmata
in testes of halfbeaks of the genus Zenarchopterus
(Teleostei: Hemiramphidae). Copeia 1987:300-311.
Grier HJ, Linton JR, Leatherland JF, deVlaming VL.
1980. Structural evidence for two different testicular
types in teleost fishes. Amer J Anat 159:331-345.
Grier HJ, Moody DP, Cowell BC. 1990. Internal fertili-
zation and sperm morphology in the brook silverside,
Labidesthes sicculus (Cope). Copeia 1990:221-226.
Grier HJ, Parenti LR. 1994. Reproductive biology and
systematics of phallostethid fishes as revealed by gonad
structure. Environ Biol Fishes 41:287-299.
Grier HJ, Uribe MC, Parenti LR, De la Rosa-Cruz G. 2005.
Fecundity, the germinal epithelium, and folliculogenesis
in viviparous fishes. In: this volume. p 191-216.
Haas V. 1993. Xiphophorus phylogeny, reviewed on the
basis of courtship behaviour. In: Schroeder JH, Bauer
J, Schartl M. editors, Trends in ichthyology. Blackwell,
London. p 279-288.
Hamilton A. 2001. Phylogeny of Limia (Teleostei: Poeci-
liidae) based on NADH dehydrogenase subunit 2 se-
quences. Mol Phyl Evol 19:277-289.
Hrbek T, Larson A. 1999. The evolution of diapause in the
killifish family Rivulidae (Atherinomorpha, Cyprin-
odontiformes): A molecular phylogenetic and biogeo-
graphic perspective. Evolution 53:1200-1216.
Hrbek T, Meyer A.. 2003. Closing of the Tethys Sea and
the phylogeny of Eurasian killifishes (Cyprinodonti-
formes: Cyprinodontidae). J Evol Biol 16(1):17-36.
Johnson GD, Patterson C. 1993. Percomorph phylogeny:
a survey of acanthomorphs and a new proposal. Bull
Mar Sci 52:554-626.
Klie K. 1988. Morphologische und histologische Unter-
suchungen an neuem Adrianichthys-Material ? Ein
Beitrag zur Systematik und Verwandschaft der Adrian-
ichthyidae (Pisces: Atheriniformes). Diplomarbeit,
Universit?t, Hamburg.
Kottelat M. 1990a. Synopsis of the endangered Buntingi
(Osteichthyes: Adrianichthyidae and Oryziidae) of
Lake Poso, Central Sulawesi, Indonesia, with a new
reproductive guild and descriptions of three new spe-
cies. Ichthyol Explor Freshwaters 1:49-67.
Kottelat M. 1990b. The ricefishes (Oryziidae) of the
Malili lakes, Sulawesi, Indonesia, with description of
a new species. Ichthyol Explor Freshwaters 1:151-166.
Kottelat M, Whitten AJ, Kartikasari SN, Wirjoatmodjo
S. 1993. Freshwater fishes of Western Indonesia and
Sulawesi. Hong Kong: Periplus Editions (HK) Ltd. in
collaboration with the Environmental Management
Development in Indonesia (EMDI) Project, Ministry
of State for Population and Environment, Republic of
Indonesia, Jakarta.
Kulkarni CV. 1940. On the systematic position, structural
modifications, bionomics and development of a re-
markable new family of cyprinodont fishes from the
province of Bombay. Rec Indian Mus 42:379-423.
Lazara KJ. 2001. The killifishes: an annotated checklist,
synonymy and bibliography of recent oviparous cy-
prinodontiform fishes: The Killifish Master Index,
Fourth Edition. American Killifish Association, Cin-
cinnati, OH.
? Viviparous Fishes
 Systematics, Biogeography, and Evolution28
Li SZ. 2001. On the position of the suborder Adrian-
ichthyoidei. Acta Zootax Sin 26:583-588.
Loureiro M, deS? RO. 1996. External morphology of the
chorion of the annual fishes Cynolebias (Cyprinodon-
tiformes: Rivulidae). Copeia 1996:1016-1022.
Loureiro M, deS? RO. 1998. Osteological analysis of the
killifish genus Cynolebias (Cyprinodontiformes: Ri-
vulidae). J Morph 1998:245-262.
Lovejoy NR. 2000. Reinterpreting recapitulation: system-
atics of needlefishes and their allies (Teleostei: Beloni-
formes). Evolution 54:1349-1362.
Lovejoy N, Collette BB. 2001. Phylogenetic relationships
of the new world needlefishes (Teleostei: Belonidae)
and the biogeography of transitions between marine
and freshwater habitats. Copeia 2001:324-338.
Lovejoy NR, Iranpour M, Collette BB. 2004. Phylogeny
and ontogeny of beloniform fishes. Integr Comp Biol
44:366-377.
L?ssen A, Falk TM, Villwock W. 2003. Phylogenetic pat-
terns in populations of Chilean species of the genus
Orestias (Teleostei: Cyprinodontidae): results of mito-
chondrial DNA analysis. Mol Phyl Evol 29:151-60.
Lydeard C. 1993. Phylogenetic analysis of species richness:
has viviparity increased the diversification of actino-
pterygian fishes? Copeia 1993:514-518.
Lydeard C, Wooten MC, Meyer A. 1995. Cytochrome b
sequence variation and a molecular phylogeny of the
live-bearing fish genus Gambusia (Cyprinodonti-
formes: Poeciliidae). Can J Zool 73:213-227.
Marcus JM, McCune AR. 1999. Ontogeny and phylog-
eny in the northern swordtail clade of Xiphophorus.
Syst Biol 48:491-522.
Martin KL. 1999. Ready and waiting: delayed hatching
and extended incubation of anamniotic vertebrate
terrestrial eggs. Amer Zool 39:279-288.
Mart?nez VH, Monasterio de Gonzo GAM. 2002. Testis
morphology and spermatozeugma formation in Jenyn-
sia multidentata. In: Meeting book, II International
Symposium on Livebearing Fishes. Abstract. Quer?-
taro, Qro., Mexico.
Meisner AD. 2001. Phylogenetic systematics of the
viviparous halfbeak genera Dermogenys and Nomor-
hamphus (Teleostei: Hemiramphidae: Zenarcho-
pterinae). Zool J Linn Soc 133 (2): 199-283.
Meisner AD, Burns JR. 1997a. Testis and andropodial
development in a viviparous halfbeak, Dermogenys sp.
(Teleostei: Hemiramphidae). Copeia 1997:44-52.
Meisner AD, Burns JR. 1997b. Viviparity in the halfbeak
genera Dermogenys and Nomorhamphus (Teleostei:
Hemiramphidae). J Morph 234:295-317.
Meisner AD, Collette BB. 1999. Generic relationships of the
internally-fertilized southeast Asian halfbeaks (Hemi-
ramphidae: Zenarchopterinae). In: S?ret B, Sire JY, edi-
tors, Proceedings of the 5th Indo-Pacific Fish Conference,
Noum?a, 1997. Soc Fr Ichtyol, Paris. p 69-76.
Meyer A, Lydeard C. 1993. The evolution of copulatory
organs, internal fertilization, placentae and viviparity
in killifishes (Cyprinodontiformes) inferred from a
DNA phylogeny of the tyrosine kinase gene X-src. Proc
R Soc Lond B 254:153-162.
Meyer A, Morrissey JM, Schartl M. 1994. Recurrent ori-
gin of a sexually selected trait in Xiphophorus fishes in-
ferred from molecular phylogeny. Nature 386:539-542.
Miya M, Takeshima H, Endo H, Ishiguro NB, Inoue JG,
Mukai T, Satoh TP, Yamaguchi M, Kawaguchi A,
Mabuchi K, Shirai SM, Nishida M. 2003. Major
patterns of higher teleostean phylogenies: a new per-
spective based on 100 complete mitochondrial DNA
sequences. Mol Phyl Evol 26:121-138.
Mojica CL, Meyer A, Barlow GW. 1997. Phylogenetic
relationships of species of the genus Brachyrhaphis
(Poeciliidae) inferred from partial mitochondrial
DNA sequences. Copeia 1997:298-305.
Morris MR, de Queiroz K, Morizot DC. 2001. Phyloge-
netic relationships among populations of northern
swordtails (Xiphophorus) as inferred from allozyme
data. Copeia 2001:65-81.
Murphy WJ, Collier GE. 1997. A molecular phylogeny
for aplocheiloid fishes (Atherinomorpha, Cyprin-
odontiformes): the role of vicariance and the origins of
annualism. Mol Biol Evol 14: 790-799.
Murphy WJ, Collier GE. 1999. Phylogenetic relation-
ships of African killifishes in the genera Aphyosemion
and Fundulopanchax inferred from mitochondrial
DNA sequences. Mol Phyl Evol 11:351-360.
Murphy WJ, Nguyen TNP, Taylor EB, Collier GE.
1999a. Mitochondrial DNA phylogeny of West Afri-
can aplocheiloid killifishes (Cyprinodontiformes,
Aplocheilidae). Mol Phyl Evol 11:343-350.
Murphy WJ, Thomerson JE, Collier GE. 1999b. Phylog-
eny of the neotropical killifish family Rivulidae (Cy-
prinodontiformes, Aplocheiloidei). Mol Phyl Evol
13:289-301.
Nelson JS. 1984. Fishes of the World, Second Edition.
John Wiley and Sons.
Nelson JS. 1994. Fishes of the World, Third Edition. John
Wiley and Sons.
Parenti LR. 1981. A phylogenetic and biogeographic
analysis of cyprinodontiform fishes (Teleostei, Ather-
inomorpha). Bull Amer Mus Nat Hist 168:335-557.
Parenti LR. 1984a. A taxonomic revision of the Andean
killifish genus Orestias (Cyprinodontiformes, Cyprin-
odontidae). Bull Amer Mus Nat Hist 178: 107-214.
Parenti LR. 1984b. On the relationships of phallostethid
fishes (Atherinomorpha), with notes on the anatomy
of Phallostethus dunckeri Regan, 1913. Amer Mus
Novit No. 2779. 12 p.
Parenti LR. 1987. Phylogenetic aspects of tooth and jaw
structure of the medaka, Oryzias latipes, and other
beloniform fishes. J Zool London 211:561-572.
Lynne R. Parenti ?
The Phylogeny of Atherinomorphs. Reproductive System 29
Parenti LR. 1989a. Why ricefish are not killifish. J Amer
Killifish Assoc 22(3):79-84.
Parenti LR. 1989b. A phylogenetic revision of the phal-
lostethid fishes (Atherinomorpha, Phallostethidae).
Proc Cal Acad Sci 46:243-277.
Parenti LR. 1993. Relationships of atherinomorph fishes
(Teleostei). Bull Mar Sci 52:170-196.
Parenti LR, Song J. 1996. Phylogenetic significance of the
pectoral/pelvic fin association in acanthomorph fishes:
A reassessment using comparative neuroanatomy. In:
Stiassny MLJ, Parenti LR, Johnson GD, editors, Inter-
relationships of fishes, Academic Press, San Diego.
p 427-444.
Parenti LR, Grier HJ. 2004. Evolution and phylogeny of
gonad morphology in bony fishes. Integr Comp Biol
44:333-348.
Parker A. 1997. Combining molecular and morphologi-
cal data in fish systematics: examples from the Cyprin-
odontiformes. In: Kocher TD, Stepien CA, editors,
Molecular Systematics of Fishes, Academic Press, San
Diego. p 163-188.
Parker A, Kornfield I. 1995. A molecular perspective on
evolution and zoogeography of cyprinodontid killi-
fishes. Copeia 1995:8-21.
Rauchenberger M. 1989. Systematics and biogeography
of the genus Gambusia (Cyprinodontiformes: Poeci-
lidae [sic]). Amer Mus Novit No. 2951. 74 p.
Roberts CD. 1993. Comparative morphology of spined
scales and their phylogenetic significance in the
Teleostei. Bull Mar Sci 52:60-113.
Rodr?guez CM. 1997. Phylogenetic analysis of the tribe
Poeciliini (Cyprinodontiformes: Poeciliidae). Copeia
1997:663-679.
Rosen DE. 1964. The relationships and taxonomic posi-
tion of the halfbeaks, killifishes, silversides and their
relatives. Bull Amer Mus Nat Hist 127:217-268.
Rosen DE, Bailey RM. 1963. The poeciliid fishes (Cy-
prinodontiformes), their structure, zoogeography, and
systematics. Bull Amer Mus Nat Hist 126:1-176.
Rosen DE, Parenti LR. 1981. Relationships of Oryzias,
and the groups of atherinomorph fishes. Amer Mus
Novit No. 2719. 25 p.
Saeed B, Ivantsoff W, Allen GR. 1989. Taxonomic revi-
sion of the family Pseudomugilidae (Order Ather-
iniformes). Aust J Freshwater Res 40:719-787.
Saeed B, Ivantsoff W, Crowley LELM. 1994. Systematic
relationships of atheriniform families within Division
I of the Series Atherinomorpha (Acanthopterygii) with
relevant historical perspectives. Voprosi Ikhtiologii
34(4):1-32.
Schartl M. 1995. Platyfish and swordtails: a genetic sys-
tem for the analysis of molecular mechanisms in tu-
mor formation. Trends Genet 11:185-189.
Stiassny MLJ. 1990. Notes on the anatomy and relation-
ships of the bedotiid fishes of Madagascar, with a
taxonomic revision of the genus Rheocles (Atherino-
morpha: Bedotiidae). Amer Mus Novit No. 2979. 33 p.
Stiassny MLJ. 1993. What are grey mullets? Bull Mar Sci
52:197-219.
Stiassny MLJ, Moore JA. 1992. A review of the pelvic
girdle of acanthomorph fishes, with comments on
hypotheses of acanthomorph interrelationships. Zool
J Linn Soc 104:209-242.
Tsuneki K. 1992. A systematic survey of the occurrence of
the hypothalamic saccus vasculosus in teleost fish.
Acta Zool 73:67-77.
Webb SA, Graves JA, Mac?as-Garcia C, Magurran AE,
Foighil DO, Ritchie MG. 2004. Molecular phylog-
eny of the livebearing Goodeidae (Cyprinodonti-
formes). Mol Phyl Evol 30:527-544.
Weber M, de Beaufort LF. 1922. Family Adrianichthyi-
dae. In: IV. Heteromi, Solenichthyes, Synentognathi,
Percesoces, Labyrinthici, Microcyprini. The Fishes of
the Indo-Australian Archipelago. EJ Brill, Leiden. p
376-381.
White BN, Lavenberg RJ, McGowen GE. 1984. Ather-
iniformes: development and relationships. In: Moser
HG, Richards WJ, Cohen DM, Fahay MP, Kendall
AW, Jr., Richardson SL, editors, Ontogeny and sys-
tematics of fishes. Special Publication No. 1, Supple-
ment to Copeia, American Society of Ichthyologists
and Herpetologists. p 355-362.
Wiley EO, Johnson GD, Dimmick WW. 2000. The in-
terrelationships of acanthomorph fishes: A total evi-
dence approach using molecular and morphological
data. Biochem Syst Ecol 28: 319-350.
Wourms JP. 1972. The developmental biology of annual
fishes. III. Pre-embryonic and embryonic diapause of
variable duration in the eggs of annual fishes. J Exp
Zool 182:389-414.
Wourms JP. 1976. Annual fish oogenesis. I. Differentia-
tion of the mature oocyte and formation of the pri-
mary envelope. Dev Biol 50:338-354.
Wourms JP, Sheldon H. 1976. Annual fish oogenesis. II.
Formation of the secondary egg envelope. Dev Biol
50:355-366.
Yamamoto T. 1975. Medaka (Killifish) Biology and
Strains. Series of Stock Culture in Biological Field.
Keigaku Publishing Company, Tokyo.
? Viviparous Fishes
 Systematics, Biogeography, and Evolution30