Reprinted from
THE TEXAS JOURNAL OF SCIEN
Vol.
56
Relative Variability of Hybrids between the Minnows,
Notropis lepidus and N. proserpinus
by CLARK HUBBS
The University of Texas
Interspecific fish hybrids are normally intermediate between their
parental species (Carl L. Hubbs, Laura C. Hubbs, and R. E. Johnson,
1943, and Carl L. Hubbs, 1955). In the latter paper, the author also
pointed out that the taxonomic characters of some F, hybrids do not
normally grade into the taxonomic characters of either parental
species. Clark Hubbs and Strawn (in press, b) discussed a group of F,
hybrids between Etheostoma spectabile ( Agassiz) and Percina caprodes (Rafinesque) which are much more variable than their parental
species in most taxonomic characters and grade into the parental types
in those characters which vary most. Not only are these hybrids more
variable but also they are somewhat extreme to the parental species in
some taxonomic characters. A single sample of F, hybrids between two
closely related minnows, Notropis lepidus (Girard) and Notropis
proserpinus (Girard), also is not only more variable than any available sample of either parental species but also greatly exceeds the
parental species in one taxonomic character.
In contrast to the E. spectabile x P. caprodes hybrids, which are between distantly related parents, the two parental species of this cross
(N. lepidus and N. proserpinus) are closely related. Gene flow between
the two species is genetically possible; however, the present known
ranges are entirely allopatric. Notropis proserpinus (here considered
to include several allopatric populations, which may be distinct
species) is known to inhabit clear spring-fed streams in Texas, New
Mexico, Nuevo Leon, Coahuila, and Chihuahua, that are tributary to
the Rio Grande. Notropis lepidus is known from the clear spring-fed
headwaters of the Edwards Plateau (Clark Hubbs, 1954) . This latter
species is closely related and allopatric to N. lutrensis (Baird and
Girard) . Selective mating tests have not been carried out to test the
validity of the specific distinction between the two forms. Notropis
lutrensis is sympatric with N. proserpinus and no natural hybrids are
known. (Carl L. Hubbs, 1955, reported only artificial hybrids between
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THE TEXAS JOURNAL OF SCIENCE
members of the subgenus Moniarza, in which he included the three
nominal species. This artificial hybridization is based on this cross.)
In any case, therefore, the N. lepidus x N. proserpinus cross is interspecific.
I wish to thank Mr. Kirk Strawn who has read and criticized this
manuscript. The problem has been discussed with Drs. W. Frank
Blair, Carl L. Hubbs, and Wilson Stone.
MATERIALS AND METHODS
The Notropis proserpinus sample was collected by Clark Hubbs and
Kirk Strawn from Dolan Creek at Dolan Springs, 36 miles north-northwest of Del Rio, Val Verde County, on May 18, 1953.
The Notropis lepidus wild sample was collected by Clark Hubbs
and Kirk Strawn from Montell Creek six miles northwest of Monte%
Uvalde County, Texas, on December 28, 1952, and on June 20, 1953.
The Notropis lepidus control sample is composed of 25 laboratory
raised individuals. On December 7, 1953, approximately 30 young
were removed from a stock tank of N. lepidus collected with the wild
sample. These laboratory raised fish often were observed in courtship
behavior, but only three young were obtained. The sample was preserved in September 1955.
The hybrid sample is composed of 26 laboratory raised individuals.
Approximately 30 individuals were noted on January 28, 1954, in an
aquarium from which two male N. proserpinus, collected with the
N. proserpinus sample, and two females of the parental stock of the
N. lepidus control sample had been removed. These laboratory raised
individuals have been observed in courtship behavior, but no young
have been found in the tank. Only one of 14 females has developing
eggs in the ovary. The others have reduced ovaries like those of the
E. spectabile x P. caprodes hybrids reported by Clark Hubbs and
Strawn (in press, b) . The nuptial tubercles of many of the males are
less pronounced than those of the parental species. The sample was
preserved in September, 1955.
The counting methods are those outlined in Carl L. Hubbs and
Lagler ( 1947) .
ANAL RAYS
The greatest amount of relative variation of any meristic character
of the hybrids is in the number of anal rays (Table I) . The degree of
variance is two to three times as great as that of any of the parental
stocks analyzed. Moreover, the hybrids average five to six more rays
than any parental stock. The anterior anal rays are normally spaced
and the posterior ones crowded. The highest recorded number of anal
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VARIABILITY OF HYBRID MINNOWS
rays for any member of the genus that I know of is 13 reported for
Notropis signipinnis Bailey and Suttkus (1952) and this number is
far exceeded by many of the anal ray counts of the hybrids. Although
the control sample of N. lepidus is slightly more variable than the wild
sample, it is possible that the increased variation is due to chance. The
increased average number of anal rays of the control sample probably
is due to differences between laboratory and field conditions. Other
samples of N. lepidus have more rays than the Monte11 wild sample.
A low number of anal rays in the hybrids apparently is not correlated with increased fertility, i.e., the ripe female has 17 anal rays and
the males with greatest development of secondary sexual characters
have similar counts to those that have the least development of those
characters.
DORSAL RAYS
The variation of the number of dorsal rays in the hybrid sample is
greater than that of any parental sample analyzed (Table II) . The
average number of dorsal rays exceeds that of the parental stocks.
Moreover, all species in the genus Notropis that I know of normally
have eight dorsal rays as a modal number, while these hybrids have
nine dorsal rays as the mode. The wild and laboratory samples of N.
lepidus are very similar in all statistical computations for dorsal ray
TABLE I
Anal Rays
Mean
Notropis proserpinus. ..... 8.10
Hybrids .............................. 14.65
Notropis lepidus control. 9.52
Notropis lepidus wild ..... 8.47
Mini- Maximum mum Standard Standard
Number Number Deviation Error Variance
7
9
8
8
9
20
11
9
0.43
3.03
0.71
0.50
0.038
0.595
0.143
0.067
0.053
0.207
0.075
0.059
TABLE II
Dorsal Rays
Mean
Notropis proserpinus...
Hybrids ..............................
Notropis lepidus control.
Notropis lepidus wild .....
8.01
8.62
7.96
7.86
Mini- Maximum mum Standard Standard
Number Number Deviation Error Variance
7
8
7
7
9
10
9
8
0.19
0.57
0.35
0.35
0.022
0.112
0.070
0.050
0.024
0.066
0.044
0.045
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THE TEXAS JOURNAL OF SCIENCE
number. There is no correlation between the number of dorsal and
anal rays or between the number of dorsal rays and fertility of the
hybrids.
PELVIC FIN
Only two of the 26 hybrids have normal pelvic fins. One has a degenerate left pelvic and no right pelvic. The other 23 have no pelvics.
The two hybrids with normal pelvic fins have low anal ray counts of
9 and 10, near those of the parental species. Only one of the many
examined specimens of the parental species has no pelvics. This individual, in the N. lepidus control sample, has 11 anal rays, among the
extreme counts for this fin in that sample. Apparently the absence
of pelvic fins is correlated with increased number of anal fin rays.
LATERAL LINE SCALES
Although the number of lateral line scales varies most in the hybrid
sample (Table III), it is possible that this increased variation is due to
chance. Other samples of N. lepidus have a variation approximating
TABLE III
Lateral Line Scales
Mean
Notropis proserpinus... 35.39
35.81
Hybrids
Notropis lepidus control. 35.28
Notropis lepidus wild .... 34.04
Mini- Maximum mum Standard Standard
Number Number Deviation Error Variance
34
34
34
31
38
39
37
36
0.82
1.10
0.68
0.88
0.073
0.215
0.136
0.124
0.023
0.031
0.019
0.025
that of the hybrids. The average number of scales of the hybrids is
higher than that of any parental sample. I believe that this is due to
laboratory conditions as the N. lepidus controls average more than one
more lateral line scale than the wild stock. If laboratory conditions
add one lateral line scale to the number present in wild stocks, the
hybrids are approximately intermediate.
DISCUSSION
The single F, hybrid sample of Notropis lepidus x N. proserpinus
is markedly more variable than any examined control sample in some
taxonomic characters. The increased variability may be due to genetic
causes or may result from abnormal developmental conditions in the
laboratory. Three possible genetic causes for such increased variability
of F, hybrids have been suggested by Clark Hubbs and Strawn (in
VARIABILITY OF HYBRID MINNOWS
467
press, b) . (1) Previous introgression, which would result in chromosome segments of one species being transferred to the other, these segments being suppressed in the pure species, and the recombination of
the chromosome segments in the hybrid permitting the expression of
all stages between those of the parental species. Clark Hubbs and
Strawn (in press, b) discounted introgression in Etheostoma spectabile
x Percirza caprodes hybrids as they doubted that the hybrids are fertile.
These Notropis hybrids, however, are probably somewhat fertile. One
female has apparently viable eggs and some males have well developed secondary sexual characters. Courtship behavior has been
noted but no young have been observed. This is not surprising as members of the genus Notropis are voracious egg eaters and few young
have survived in most tanks containing these fishes (Clark Hubbs and
Strawn, in press, a) . In this same paper possible gene flow between
two closely related species, N. lutrensis and N. venustus (Girard) , is
shown. However, according to presently known ranges the parental
forms for these variable hybrids are allopatric. All of the characters of
these hybrids that vary widely are extreme to those of the parental
species. (2) Modifying genes, which would influence the meristic
characters of one species to approach the average number of that
parental species in hybrids, and again result in all intermediate stages
between the parental species. Likewise, this does not fit as the hybrid
counts that vary most are extreme to the counts of the parental species.
(3) Variation in developmental rates, which assumes that a character
is formed during a given ontogenetic period, that the length of that
period controls the degree of expression of that character, that the
ontogenetic period at which certain characters develop differs in the
two parental species, and that the hybrids may begin the development
of the character at the point of inflection (Martin, 1949) of the first
species and stop the development of the character at the point of inflection of the other or at any intermediate stage. Thus, many degrees
of expression are possible, including those extreme to the phenotypes
of the parental species. Variations of the point of inflection may have
been introduced by introgression. Differences between the ontogenetic
periods at which certain characters develop has not been demonstrated
in closely related species of any group of fishes. However, different
effects of similar environmental conditions are indicated by Clark
Hubbs and Springer (ms.) for closely related species of Gambusia. A
large amount of experimental work is necessary before this theory
can be verified.
It is also possible that the excessive variation of hybrids may be
caused by environmental conditions present in the laboratory. Taning
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THE TEXAS JOURNAL OF SCIENCE
(1952) has reviewed literature on the effect of varying environmental
conditions on the phenotypes of many fishes. He has pointed out that
extremely high environmental temperatures may result in the absence
of pelvic fins. Laboratory temperatures in the winter, however, approximate the lower temperatures recorded for naturally spawning
parental stocks. Likewise, the high and variable anal ray counts of
the hybrids may be due to laboratory environmental conditions.
Weisel (1955) demonstrated that the anal ray count of another minnow, Richardsonius balteatus (Richardson) , is inversely correlated
with temperature. However, his samples with the largest numbers of
anal rays are not appreciably more variable than those with fewer
anal rays. The average number of anal rays of the laboratory raised
sample of N. lepidus is approximately one more than the wild sample,
which developed at warmer temperatures. However, the variability of
the control sample is not appreciably increased over that of the wild
sample. Therefore, one of the five or six added anal rays can be attributed to environmental modifications of the phenotype, but the
others remain unexplained as is the increased variability. Moreover,
the bulk of the evolutionary data indicate that addition of structures is
more difficult than loss of the structure.
The hybrids discussed by Clark Hubbs and Strawn (in press, b)
differ from the controls in that fertilization of the hybrid eggs may
have been delayed more than that of the controls. It is likewise possible that the Notropis lepidus eggs fertilized with N. proserpinus
sperm may not have been fertilized as quickly as if they were fertilized with N. lepidus sperm. The urogenital papillae may not have
been so closely approximated in interspecific matings as in intraspecific matings.
I strongly suspect that the increased variability and extreme phenotypic expression of the hybrids is due to the combination of the dissimilar developmental rates resulting from the interaction of the
genetic components of the parental species. Newman (1908) has
pointed out that F, Fundulus hybrids also are more variable than
their controls, and Gordon and Rosen (1951) report a high degree of
variability in FI Xiphophorus hybrids in some characters.
LITERATURE CITED
BAILEY, REEVE M., AND ROYAL D. Surmus, 1952—Notropis signipinnis, a new
cyprinid fish from southeastern United States. Occ. Pap. Univ. Mich. Mus. Zool.,
542: 1-15, 2 pls.
GORDON, MYRON, AND DONN E. ROSEN, 1951—Genetics of species differences in the
morphology of the male genetalia of Xiphophorine fishes. Bull. Am. Mus. N at.
Hist., 95: 413-464, pls. 17-18.
VARIABILITY OF HYBRID MINNOWS
469
Hums, CARL L., 1955—Hybridization between fish species in nature. Systematic
Zoology, 4: 1-20.
HUBBS, CARL L., LAURA C. HUBBS, AND RAYMOND E. JOHNSON, 1943—Hybridization
in nature between species of catostomid fishes. Contr. Lab. Vert. Biol. Univ.
Mich., 22: 1-76, pls. 1-7.
Iltiass, CARL L., AND KARL F. LAGLER, 1947—Fishes of the Great Lakes Region.
Crarzbrook Inst. Sci., 26: i-xi + 1-186,2-6 pls.
Hum's, CLARK, 1954—Corrected distributional records for Texas fresh-water fishes.
Tex. Jour. Sci., 6: 277-291.
HUBBS, CLARK, AND VICTOR G. SPRINGER, MS—Three new fishes of the Gambusia
rzobilis species group with notes on their ecology and evolution.
Husas, CLARK, AND KIRK STRAWN, in press, a—Interfertility between two sympatric
fishes, Notropis lutrensis and Notropis verzustus (Cyprinidae). Evolution.
in press, b.—Relative variability of hybrids between the darters,
Etheostoma spectabile and Percina caprodes. Evolution.
MARTIN, W. R., 1949—The mechanics of environmental control of body form in
fishes. Univ. Toronto Studies, Biol. Ser., 58: 1-91.
NEWMAN, H. H., 1908—The process of heredity as exhibited by the development of
Fundulus hybrids. J. E. Z., 5: 503-561,5 pls.
TANING, A. V., 1952—Experimental study of meristic characters in fishes. Biol.
Rev., 27: 169-193.
WEISEL, GEORGE F., 1955—Variations in the number of fin rays of two cyprinid
fishes correlated with natural water temperatures. Ecology, 36: 1-6.