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The American Naturalist
Vo\.I13,No.6
THE EVOLUTION OF LIVE-BEARING
LIZARDS AND SNAKES
June 1979
IN
RICHARD SHINE. AND J. J. BULL
Department
of Biology, University
of Utah, Salt Lake City, Utah
84112
Most reptiles lay eggs, but many lizards and snakes are live-bearers. Taxonomic
and embryological evidence indicates that egg-laying is ancestral (Weekes 1935;
Matthews 1955; Amoroso 1960), so the common occurrence of genera containing
both live-bearers and egg-layers shows that live-bearing has arisen from egg-laying
several times (table 1). This paper considers the ecological conditions favoring the
evolution of live-bearing in squamate reptiles. There have been several excellent
treatments of reptilian live-bearing which have made this current synthesis possible
(Melll929, Weekes 1935; Sergeev 1940; NeillI964, 1971; Packard 1966; Greer 1968;
Fitch 1970; Greene 1970; Packard et a\. 1977; Tinkle and Gibbons 1977). Here a
comprehensive model is presented to account for the evolutionary origin of livebearing, and published data are used to test predictions from the mode\.
ORIGIN VERSUS MAINTENANCE
The evolution of live-bearing from egg-laying in squamate reptiles is almost
certainly a grad ual process. In the early stages of this process, females carry the eggs
long enough to permit some embryonic development in utero but lay the eggs prior
to the completion of embryogenesis. Continued selection for progressively longer egg
retention eventually results in complete intrauterine incubation (live-bearing).
Certain physiological and anatomical changes must accompany the transition
from egg-laying to live-bearing (Weekes 1935; Bauchot 1965; Yaron 1972). These
requirements probably prevent any rapid evolutionary "jump" from egg-laying
(without in utero development) to live-bearing. For example, the female must
develop vascular structures for gaseous exchange between oviducts and offspring,
and she must maintain only a thin egg shell around them while they are in utero.
These modifications must be l1ore extensively developed in females that retain eggs a
long time than in females tLat retain eggs only a short time, because the need for
exchange between mother and offspring increases as the embryos become larger
(DmieI1970). Thus, even females capable of retaining eggs for short intervals are not
necessarily capable of sustaining eggs in utero throughout development. Packard et
a\. (1977) also provide supporting evidence for these assumptions.
In order for live-bearing to arise from egg-laying, selection must favor the
intermediate stages in which females retain eggs for progressively longer periods of
* Present address: ZoQlogy Department, University of Sydney, New South Wales 2006, Australia.
Am. Nat. 1979. Vol. 113. pp. 905-923.
,1') 1979 by The University of Chicago. 0003-0147(79/1306-0009$01.65
906
THE AMERICAN NATURALIST
time. There may be circumstances in which it is advantageous to be live-bearing, but
in which the intermediate stages of egg retention are not favored (Weekes 1935;
Tinkle 1967; Packard et al. 1977; Tinkle and Gibbons 1977). A major difference
between a live-bearing female and an intermediate egg-retaining female is that the
live-bearer is emancipated from nesting while the intermediate female is not. If the
act of nesting is strenuous or risky, then an advantage accrues to live-bearing but not
to the intermediate stages of egg retention. In discussing the evolution of live-bearing
it is therefore necessary to distinguish forces which provide an advantage for these
intermediate stages (i.e., favoring the origin) from forces which merely provide an
advantage for the maintenance of live-bearing. This paper investigates only the origin
of live-bearing. The maintenance of live-bearing is considered by Sergeev (1940),
Tinkle and Gibbons (1977), and Shine and Berry (1978).
ECOLOGY
How will selection act upon a female carrying her eggs slightly longer than the
average female, thus allowing the young to develop in utero and spend less time in
the nest? The fitness parameters most likely to be affected by oviducal retention are
(1) offspring survival, an~ (2) mother survival and future fecundity. Egg retention is
most likely to be favored when either (i) the survival of young is greatly improved by
oviducal retention, or (ii) the mother does not lower her future fecundity if she carries
the eggs longer (Appendix). Some ecological factors which may favor egg retention in
the;:seways are discussed below. Also, we attempt to distinguish factors which can
select for the complete evolution of live-bearing from factors which select only for
short intervals ?f egg retention.
Factors Affecting Egg Survival
1. Temperature.-Proper embryonic development in squamate reptiles requires a
limited range of temperatures, and temperature extremes may be fatal (Fitch 1964;
Licht and Moberly 1965; Vinegar 1974). Also, the rate of embryonic development is
proportional to temperature in some species (Blanchard and Blanchard 1941; Fitch
1954; Platt 1969). The fitness of hatchlings therefore depends upon incubation
temperature to the extent that embryogenesis must be normal and hatching occurs
during some optimal time. Certainly the mother should lay eggs in the sites which are
most thermally suitable for development, but some environments may be so extreme
that ideal nest sites are not available and eggs will inevitably be exposed to
non optimal temperatures. Such thermal unsuitability may be, characteristic of cold
environments and possibly of hot environments.
Cold environments may adversely affect the fitness of hatchlings for the two
reasons outlined above: (a) The nest substrate may be cold enough to harm embryos,
and (b) the cold nest may slow development so that hatching occurs later than some
optimal time. These two effects are not necessarily independent, but the distinction is
useful. As an example of (a), eggs might be laid early enough in the spring to be
subjected to late frosts. For (b), montane and some temperate environments could be
too cool to permit spring-laid eggs to hatch sufficiently long before winter.
EVOLUTION
OF LIVE-BEARING
907
Cold environments are unique in that short intervals of egg retention may
overcome athermal complications during development. In the example of (a), egg
retention would avoid exposure of eggs to the frosts, since the mother could seek
shelter at frost-free depths. In the example of (b), egg retention would lead to early
hatching if the mother maintained a body temperature higher than substrate
temperature during part of the day. When laid, embryos would be developed further
than if they had remained in the ground during the same interval. It is in fact known
that females of some species accelerate development by thermoregulating when they
retain eggs, and thus hasten hatching (Sergeev 1940; Blanchard and Blanchard 1941;
Stewart 1965; Hirth and King 1969; Osgood 1970; Packard et al. 1977). Cold
environments need not always favor egg retention, though. The time of hatching
cannot be hastened if the development Tate is temperature-independent (e.g., Chelydra, Yntema 1968) or if the mother maintains the same temperature as the substrate
(aquatic or fossorial species, Brattstrom 1965).
Cold environments should therefore often select for egg retention, as suggested
previously (Mell 1929; Weekes 1935; Sergeev 1940; Packard 1966; Greer 1966;
Packard et al. 1977). In addition, cold environments favor the progressive evolution
to live-bearing because they often occur as gradients from warm to cold habitats,
with latitude or altitude. As populations of individuals that retain eggs become
established in cool areas, selection can favor increased retention times among the
invaders of even cooler areas. This can progress until live-bearing evolves.
Temperature extremes are less likely to be a problem in hot environments than in
cold environments, because hot environments usually contain many microhabitats
that do not experience harmfully high temperatures. It is conceivable, though, that
egg retention could.~volve in response to rapid seasonal changes in ground temperature, as in some deserts. A shallow nest sufficiently warm in spring may become too
warm later, before hatching. A deep nest may never become too warm, but could lead
to late hatching because it is too cool in spring. Some benefit may be derived from
retaining eggs until the environment passes through the temperature fluctuation.
This does not seem as compelling a cause for the evolution of egg retention or livebearing as cold environments, however.
2. Predation.-Predation is a source of high egg mortality in many reptiles and
therefore may lead to selection for egg retention. The benefit of retaining eggs
depends upon how predation is reduced by late laying and less time in the nest.
Conceivably, egg retention could evolve in response to predation when the risk of
predation is proportional te' the time spent in the nest. However, available data
indicate that predation is n\ t proportional to the time of incubation. In the cases
studied, predation has proven to be high just after the eggs have been laid, and
possibly high when the young emerge, but predation may be slight in between (Blair
1960; Moll and Legler 1971; Carr 1973). Egg retention will reduce predation only
slightly under these circumstances, because its only effect is to shorten the interval in
which there is little mortality. With this form of predation live-bearing will be
favored over egg-laying, but the intermediate stages of egg retention probably confer
no advantage.
3. Moisture extremes.-Some authors have proposed that the two extremes of
moisture content in the nest (wet and dry) select for live-bearing (Weekes 1935; Neill
908
THE AMERICAN NATURALIST
1964). Neill proposed that eggs laid in wet soil are subject to infection and that this
selects for live-bearing. Other possible reasons for mortality in wet or dry nests are
conceivable. Unfortunately, no meaningful discussion of these factors is yet possible
because little is known about egg mortality in wet or dry nests. It is also difficult to
draw correlations between egg retention and nest humidity because information is
lacking on the nesting sites of most species. A species that occupies a wet habitat may
be able to locate dry nesting areas, and vice versa. Even if wet or dry soil lowers egg
survival, retention need not be favored. Retention should evolve only if the mortality
falls chiefly on the early stages of embryogenesis, or on eggs that remain in the nest
slightly too long. Otherwise a reduction in time spent in the nest will not greatly
increase egg survival.
There is one case in which short intervals of egg retention may evolve because of
nesting in dry habitats. If a long dry season preceeds egg laying and rain usually
comes at the onset of nesting, then it may be advantageous to delay laying until it
rains (Gehlbach 1965). Eggs are thus laid in moist soil, possibly increasing their
survival. Egg retention per se need not offer an advantage to the eggs, but if the
timing of the rain is unpredictable and the mother must lay sQon after precipitation,
then early ovulation allows her the flexibility of laying at any subsequent time
(Steams' "bet hedging," [1976]).
Of the ecological factors which affect egg survival, a cold environment is the most
appealing cause for the evolution oflive-bearing. Although there are many sources of
egg mortality which may be improved slightly by retention, cold environments are
unique in that (i) they can be lethal to embryos, (ii) they can be compensated for by
short increases in retention time, and (iii) they occur in graded elines, allowing
progressive evolution to live-bearing. Mortality sources which are proportional to
the time spent in the nest do not have as high a benefit/cost ratio for egg retention.
Factors Affecting the M other
A female laden with eggs is less efficient at locomotion and, hence, may be more
vulnerable to predators and less able to forage than if she had laid the eggs (Fitch
1970; Tryon and Hulsey 1976). Egg retention is perhaps most disadvantageous to
mothers of species in which females move about actively after laying eggs. If the
female did not retain eggs, she could be moving about and feeding sooner. However,
there are many species in which the female coils around the eggs and stays with them
throughout incubation. These "brooding" females usually do not feed during this
time (FitzSimons 1919; Pope 1935; Fitch 1954; Sweeney 1961; T.aylor 1965; Leakey
1969). Retention may not be costly to such a female, because it does not prolong the
interval in which she abstains from feeding.
1. No maternalcare after laying.-Perhaps the main cost of retaining eggs is the
mother's decreased mobility. This makes her less able to feed and more vulnerable to
predation. Egg retention should be least disadvantageous in species that are least
prone to predation or that do not depend on rapid movements for feeding. Livebearing should evolve most often in species that are (1) large and deadly, because
they can ward off predators (Mell 1929; Sergeev 1940; Neill 1964); (2) secretive,
EVOLUTION
OF LIVE-BEARING
909
because they rarely encounter predators (Melll929; Fitch 1970); or (3) slow moving,
because they do not depend on speed to escape predators or to catch food (Fitch
1970). In contrast, arboreal species which rely on agility to feed or to avoid predators
should be at a greater disadvantage when retaining eggs.
The above comparisons assume that females continue to move about and feed
while retaining eggs. This is only likely to be true for short intervals of retention.
Females of many snake and lizard species become very secretive and curtail their
activities when carrying eggs for a long period, even in large and deadly species (e.g.,
the live-bearing snakes Vipera, Prestt 1971; Crotalus, Keenlyne 1972; Sistrurus,
Keenlyne and Beer 1973; Agkistrodon, Fitch and Shirer 1971; Notechis, Pseudechis,
Shine 1978). This tends to equate the cost of egg retention among the different
specIes.
Retention might evolve because of short-term events that affect the ease and safety
of nesting. For species that dig or construct nests (mainly lizards), rain may facilitate
the construction of a nest in a dry area. If nesting occurs at the time of year when
rains begin, then the female may be favored to retain eggs until rain falls (Anderson
1962). (Recall that egg survival may also be enhanced in this situation.) Long
intervals of retention need not be favored since the advantage of waiting may be
outweighed by the disadvantages of long-term retention.
2. Maternal care.-Egg retention may not be as costly to a mother if she broods
the eggs from laying until hatching: By carrying the eggs longer, she does not have to
brood them as long. This compensation means that egg retention is tnore likely to
evolve in a brooding species than in a nonbrooding species. Brooding may even favor
egg retention, but may not suffice to favor live-bearing. During the early stages of
developmcnt.,retention may be less costly than brooding, because retention allows
the mother freedom of movement to feed. As the embryos develop, the eggs increase
in volume and weight, and the mother becomes more heavily burdened (e.g., Fitch
1954; Shine 1977). Eventually, it becomes advantageous to cease moving around and
to lay the eggs.
Cold environments provide an advantage for retention in a brooding species that
does not apply to a non brooding species. In cold environments the mother's high
body temperatures can accelerate embryonic development during retention. This
shortens the total incubation period (retention plus brooding) and therefore may
decrease the mother's total interval of parental care. Live-bearing may therefore
evolve from brooding in cold environments even if egg survival is not affected.
3. Other previous hypotheses.-i) Prolonged egg retention delays the time at which
the mother can ovulate ller next clutch. This might be a major disadvantage in
species that lay more than one clutch per season (Sergeev 1940; Tinkle and Gibbons
1977)
ii) Two common arguments in the literature are that live-bearing evolves in
aquatic or arboreal species because the mother is freed from having to leave her usual
habitat in order to find a suitable nesting site (Melll929; Sergeev 1940; NeillI964;
Fitch 1970). Clearly, this does not apply to the intermediate stages (because the
mother still has to find a nest), and therefore will not lead to the evolution of
live-bearing (Packard et al. 1977). The arboreal habit may even select against the
evolution of live-bearing (see above).
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THE AMERICAN NATURALIST
PREDICTIONS
The preceding discussion yields three predictions to be tested.
I. Egg retention and live-bearing should evolve in cold climates, because egg
retention may confer advantages in avoiding lethal temperatures and in hastening
the time of hatching.
2. Egg retention and live-bearing should evolve more readily in species with
female parental care than in species without female parental care, because the costs of
egg retention to the mother are little, if at all, higher than the costs she already faces
in brooding.
3. Egg retention and live-bearing should not evolve as a response to aquatic or
arboreal life. or extremes of soil moisture, because intermediate stages of egg
retention are not favored.
Two other predictions are not tested here.
4. Egg retention may evolve most readily in large, deadly species and in secretive
species, because the mother is not vulnerable to predators. A problem in testing this
prediction is that ]arge deadly species and secretive species are likely groups to show
brooding behavior, which in itself is likely to favor egg retention.
5. Egg retention may evolve more readily in single-clutching species than in
species which produce more than one clutch per year, because egg retention does not
interfere with the mother's immediate future fecundity in single-clutching species.
This hypothesis is not tested because the data for clutch frequencies are not available
for populations showing egg retention. This test also requires separating the effect of
cold and brooding from single-clutching, because these factors will often be correlated (Fitch 1970).
TEST OF PREDICTIONS
The live-bearing habit may be favored over egg-laying under many conditions that
do 110tfavor the origin of live-bearing. Thus, the habitats occupied by live-bearing
species may often be different from the habitats in which live-bearing evolved. To test
the predictions, we must isolate the cases where live-bearing is evolving or has
evolved recently from cases in which live-bearing has a remote ancestry. This can be
done by considering the following two categories of data, also recognized by Sergeev
(1940).
i) Recent origins qf live-bearing.--Live-bearers and egg-layers co-occur within
some genera, within some subgenera or species groups, and even within some species
(table]). This indicates that there has been a transition from egg-laying to livebearing (or the reverse) subsequent to the common ancestry of these populations.
The transition from egg-laying to live-bearing is more likely than the reverse (Fitch
1970: Tinkle and Gibbons 1977), so we infer that these cases.represent origins of
live-bearing. The fact that these origins are recent (by virtue of limiting the data to
origins within a genus or smaller taxon) suggests that the ecologies of these
live-bearers may still represent the environments which favored the evolution of
live-bearing. Where live-bearers and egg-layers co-occur at higher taxonomic levels,
this supposition is not likely to be true.
EVOLUTION
911
OF LIVE-BEARING
TABLE 1
RECENT ORIGINS OF LIVE-BEARING.
Proportion
of
Live-Bearing
Species In
Cold Climat<::s
Family, Genus
Lizards
Chameleontidae
Chamaeleo ...........
3/3
Iguanidae
Corytophanes . . . . . . . . .
Lio/aemus............
Phrynosoma
... . . .
See/oporus aeneus
S. formosus group
S. sea/oris group.
.....
S. variahilis group. . . . .
Scincidae
Anoma/opus ...
Eumeees.............
Lei%pisma
(New Zealand)
(Tasmania)
.....
Anguidae
Dip/og/ossus
GerrllOnot!ls
McCoy 1968
Donoso-Barros
1966
Stebbins 1954;
Lowe and Howard
1975
1/1
2/2
1/1
1/1
Davis & Dixon
Stuart 1948;
Fitch 1970;
Werler 1951
1/1
A. E. Greer,
personal communication
Axtell 1960;
Van Devender and
Van Devender 1975;
Webb 1968;
Legler & Webb 1960
Barwick 1959;
Cogger 1975;
Rawlinson 1976;
McCann 1955
Loveridge 1942
Greer & Parker 1967
Greer 1977
Horton 1973
Smith 1935; Horton 1973
Smith 1935
+
15/15
5/5
?/I
1/1
0/4
7/10
1/1
1/1
2/3
1961;
?/1
Greer & Parker 1974;
Fitch 1970
Greer & Parker 1968
2/2
1/1
Sergeev 1940
Smith 1973
....
2/4
+
..........
9/9
+
Agamidae
Phrynoeepha/us
Authority
Schmidt & Inger 1957
1/1
13/20
3/3
3/3
Leptosial'hos .....
Lerista ..........
Lygosoma........
Mabuya (South Africa).
Mabuya (Asia) .......
Scinee/la.............
Sphenomorphus
(New Guinea) . . . . . .
Tribilonotus . . .
Lacertidae
Eremias
............
Laeerta..............
Maternal
Care Known
in Taxon?
1/1
Greer 1967;
Taylor 1956;
Lynn & Grant 1940
Stebbins 1958;
Greer 1967
Smith
1935; Minton
1966
(Continued)
EVOLUTION
911
OF LIVE-BEARING
TABLE 1
RECENT ORIGINS
Proportion
of
Live-Bearing
Species In
Cold Climate:s
Family, Genus
Lizards
Chameleontidae
Chamae/eo ......
Iguanidae
Corytophanes . . . . . . . . .
Lio/aemus . . . . .
Phrynosoma
See/oporus aeneus
S. /ormosus group
S. sea/aris group.
S. variahilis group.
Scincidae
Anoma/opus
....
..........
Eumeees .............
Leptosiaphos
Lensta
Maternal
Care Known
in Taxon?
3/3
McCoy 1968
Donoso-Barros
1966
Stebbins 1954;
Lowe and Howard 1975
111
2/2
111
111
Davis & Dixon
Stuart 1948;
Fitch 1970;
Werler 1951
I11
A. E. Greer,
personal communication
Axtell 1960;
Van Devender and
Van Devender 1975;
Webb 1968;
Legler & Webb 1960
Barwick 1959;
Cogger 1975;
Rawlinson 1976;
McCann 1955
Loveridge 1942
Greer & Parker 1967
Greer 1977
Horton 1973
Smith 1935; Horton 1973
Smith 1935
+
15/15
515
....
.
Lyyosoma........
Mabuya (South Africa).
Mabuya (Asia) ..
Seineella.............
Authority
Schmidt & Inger 1957
111
13/20
3/3
3/3
Lei%pisma
(New Zealand)
(Tasmania) ........
OF LIVE-BEAkING*
?/I
111
0/4
7/10
I11
I11
1961;
SphellOmorphus
Tribi/onotus
Lacertidae
Eremias .............
Laeerla..............
Anguidae
Dip/og/ossus . . .
?/l
Greer & Parker 1974;
Fitch 1970
Greer & Parker 1968
2/2
111
Sergeev 1940
Smith 1973
2/3
(New Guinea)
...
2/4
+
GerrllOnotus
9/9
+
Agamidae
Phrynoeepha/us
111
Greer 1967;
Taylor 1956;
Lynn & Grant 1940
Stebbins 1958;
Greer 1967
Smith
1935; Minton
1966
(Continued)
912
THE AMERICAN
NATURALIST
TABLE I (Continued)
Family, Genus
Proportion
of
Live-Bearing
Species In
Cold Climates
Maternal
Care Known
in Taxon?
?/I
+
Authority
Snakes
Typhlopidae
Typhlops
Colubridae
......
Aparallactlls
. ..
Coronella ............
Elaplre
.
..............
Helicops.
.
Oplteodrys vernalis
Sinol1atrix
...........
Viperidae
Cerastes
Echis
Vipera
Crotalidae
........
.
+
?/I
1/1
1/1
+
?/I
1/1
2/4
+
.....
2/4
+
.'
1/1
AgkistrodOI1 (Asia)
....
1940; Taylor
1965
Pitman 1974
Smith 1973; Street 1973
Pope 1935; Oliver 1959;
Fukada 1965
Rossman 1973
Ditmars 1942
Pope
1935; Smith
1973
Domergue 1959
Minton 1966;
Mendelssohn
1965;
Duff-Mackay
1965
Mendelssohn
1963
3/5
..............
Trimeresurus
0/1
1/1
1/1
Bogert
Pope 1935, Smith 1943:
Wall 1921
Pope 1935: Fukada 1964:
Nickerson
1974
Elapidae
Pseudechis
.
Covacevich
personal
& Tanner,
communication
NoTE.-Symbols: + = yes: - = no; ? = insufficientdata.
Genera.
species groups,
or species containing
populations
of egg-layers
and live-bearers
(taking
the
smallest taxon containing both types) with data on habitat. climate, and maternal care in the taxon. We
have omitted doubtful records (Tinkle and Gibbons 1977; Spellerberg 1976; Packard et al. 1977), and
cases where continents have been colonized by live-bearers.
ii) lntermediate stages of live-bearing.-Many species retain eggs long enough for
embryonic development to reach a visible state at the time of laying (table 2). These
species have progressed part of the way toward evolving live-bearing and should
therefore indicate the ecological factors favoring the evolution of live-bearing.
In order to test the hypotheses, we assembled ecological data from published
literature for live-bearers with congeneric egg-layers and for species with egg
retention (tables 1, 2). In addition, we gathered the same ecological data for over
t ,000 species which show neither live-bearing nor egg retention (table 3). These latter
data serve as an estimate of the "expected frequencies" of the various ecologies for
squamates as a whole; they form the basis for testing for a bias in the ecologies of the
live-bearers and egg-retaining species. The assignment of these species to the different
ecological categories was based on ecological descriptions in the sources (table 3,
footnote). In the absence of absolute definitions of cold climate, wet or dry habitat,
and so forth, a relative measure was used for these ecological categories in each
continental area. This no doubt introduces subjectivity into these assignments, but
no alternatives seem possible at present. Since the tests of significance are themselves
EVOLUTION
913
OF LIVE-BEARING
TABLE 2
INTERMEDIATE
STAGES OF LIVE-BEARING.
SQUAMATE SPECIES WITH EGG
DATA ON HABITAT. CLIMATE, AND MATERNAL
Population
In Cold
Climate?
Family, Species
RETENTION;
CARE IN THE SPECIES
Maternal
Care?
Authority
Lizards
Iguanidae
Ana/is aeneus
A.cybotes
...........
4.shrerei
...........
Lialaemus montieola
Sceloparus darki
S. orclltti .
S. sealaris ..
S.lIndlllalUs ............
S.rirgatus
........."...
Scincidae
.4,wtismaeeoyi..........
ElIl/leees brevi/ineatus.
...
E. callieephalus.
+
+
+
........
E./aseiatus.
..,.........
Leiolopisma guiehenoti
L.suteri
...........
L.trililleata
........
r'vforetllia boulenge;;
Scillcella laterale
SaipllOs eqllalis
Lacertidae
Locerta agilis
L. 1/1lira lis .
L. I'iridis ..
Anguidae
Diploglossus delasagra
...
Gerrhonotus mlllticarinatlls
Helodermatidae
Heloderma suspectlll/l
Agamidae
Calotes I'ersicolor
Snakes
Boidae
Pyt/ll)// molurus
Stamps 1976
Huey 1977
Huey" 1977
Donoso-Barros
1966
Kauffeld 1943; Stebbins
Stebbins 1954; 1958
Anderson 1962
Gehlbach 1965
Vinegar 1975
+
+
+
+
+
+
+
+
+
+
+
+
T.se/llege/;i
""""""
Colubridae
Alwetlllla ahaetul/a ......
Cagle 1940; Fitch
Pengilley 1972
Towns 1975
Smith 1973
Cooper 1965
Marshall 1956
+
+
1961;
1954
+
+
+
1967
Greer 1967; Taylor 1956
Stebbins 1954. 1958
Ditmars 1942. doubtful; see
Bogert & Dal Campo 1956
+
Muthukkaruppan
+
+
+
.........
Campbell & Simmons
Zweifel 1962
+
+
..
Pengilley 1972
Werler 1951
Pengilley 1972
Rawlinson 1976
Johnson 1953
Bustard 1965; Cogger
P reticulatus
P. sebae
Typhlopidae
Typhlops diardi
+
1954
?
+
+
et al. 1970
Pope 1961;
Van Mierop & Barnard 1976
Pope 1961; Fitch 1970
Joshi 1967;
Branch & Patterson 1975
Wall 1918; 1921; Smith
Taylor 1965
FitzSimons
1962
1943;
Smith 1943; Taylor
1956;
Pope 1935; Wall 1921
(Continued)
914
THE AMERICAN NATURALIST
TABLE 2 (Continued)
Population
In Cold
Climate?
Family. Species
Amplliesma sto/ata . . . . . . .
Ampltiesma rihakuri
.....
Aspidl/ra /racltyproc/a . . . .
Bnigutrignna/u
.........
C urphopltis ["ermis .......
Diadnpllis pl/llc/atus .
+
+
+
+
+
+
Eluplle dinne" . . 0. . . .
+
Eo ohso/eta
E. /uellil/ris
0.
0. 0. . . . 0.
He/i('(lpsulIgu/a/l/s
La/llprore//is
triallgull/m
LY('(IdcJ/lul//icus
Na/rixmallra
No /I<I/r;x
o..
..
.......
0..0
0
N. percarilla/a
Ol'lteadrys ["erna/is
....
f'illlOl'ltis me/(//IO/eI/CIIs.
.
Psammol'/Irlax rllOmhel/IIIS
I'salll/l1op/Jylax /ri/lIelliJlIIs
I'rrus dltwlllwdes ..
Viperidae
Ps"l/doceruste~
+
+
00000.0..
000
E. l'I"pilla
Maternal
Care?
per~!cl/S
+
+
+
+
+
+
?
+
+
+
+
?
+
+
+
+
+
Authority
WaIl 1921: Minton 1966
Fukada 1956: Malnate 1962
Wall 1921
Wall 1921
Clark 1970
Ditmars 1942: Blanchard 1930;
Fitch 1975
Fukada 1965
Ditmars 1942: Fitch 1970
Pope 1935
Zehr 1969
Rossman 1973
Ditmars 1942
WaIl 1921: Smith 1943
Duguy & Saint Girons 1966
Angel 1950; Smith 1973:
Parker 1963
Pope 1935
BIanchard 1933; Ditmars 1942:
Stille 1954; Minton 1972
Anderson 1965: Car11944
FitzSimons
1962
Sweeney 1961
Pope 1935
+
Mendelssohn
1965:
Minton 1966
+
Pope 1935; Smith 1943;
Leakey 1969
Smith 1943
Pope 1935: Wall 1921
Crotalidae
Agkis/rodc)/J UClltuS
A.
rltodosroma
Trimeresl/rtls
.
o. 0
mcm/ico/u
Elapidae
Cal/inpltis mace/el/andi
!If icrl/rtls (I/Irills
+
+
o.
+
+
+
+
Na;a/lCI;a
.
Egg retention
inferred
from short incubation
period
Soderborg 1973
Ditmars 1942: Mole 1924;
Campbell 1973
Pope 1935;
Campbell & Quinn 1975
(~ 26 days).
merely comparisons of frequencies, subjectivity in the data does not influence the
conclusions. provided we have been consistent.
1. Ure-bearillg alld egg retention should evol1"C'
ill cold climates:-If cold is a major
cause for the origin of live-bearing, then the species or populations which have
recently evolved live-bearing should be found in cold climates more often than
squamates as a whole. This prediction is supported by the cases in table 1 for which
habitat information is available (33 origins). Giving equal weight to each origin (each
entry multiplied by the proportion of live-bearers in cold) reveals that 28.1 of 33 cases
EVOLUTION
915
OF LIVE-BEARING
TABLE 3
DISTRIBUTIONS
OF SQUAMATE SPECIES WITH RESPECT TO HABITAT AND OCCURRENCE
PROPORTIONS IN EACH CATEGORY
All
Squamates
Cold climate
"""""""""'"
Wet soil.
........................
Dry soil.
........................
Aquatic. . .
..............
Arboreal.........................
Maternal
Live-Bearers in Genera
with Both Egg-Laying and
Live-Bearing Members
(n = 38)
~.14
CARE;
Species with
Egg Retention
(n = 60)
.72
.11
.13
.24
.05
.03
.02
.08
.08
.24t
.33
care
(at generic level)
.
.44(.13-.61)
.12(.04-.22)
.18(.03-.35)
.05.
(0-.14)
.10.
(.02-.28)
OF PARENTAL
................
.lIt
Based on data for 1,011 species from Africa, China, Australia, and North America. from Pitman
(1914), Pope (1935), Cogger (1915), Conant (1958), and Stebbins (1966); brackets give ranges of the four
continental means. Categories were determined by the respective authors' criteria and our personal
knowledge of the species and habitats (North America and Australia).
t Based on data for 100 egg-laying species (231 genera) in Fitch (1910).
t In egg-laying forms.
(85'/';,)are found in cold climates. This is significantly different from the proportion in
squamates as a whole (44 '\,; Fisher's exact test, P < 10- 5). Even if all of the unknown
cases in table I are assumed to inhabit warm environments, the proportion of newly
evolved live-bearers in cold climates (28.1of 38, or 74%: tables 1,3) is much higher
than among squamates in general (44%; P < .001).
Egg retention is also significantly correlated with cold climate: table 2 shows that
43 of the 60 egg-retaining species are found in cold climates, while another 15
(possibly 17) are not. Thus, the proportion of egg-retaining species found in cold
climates is significantly higher than that for squamates as a whole (72% versus 44~;";
table 3, Fisher's exact, P < 10-4).
2. Egg retention and live-bearing should evolve more readily in species with female
parental care than in species without female care.-Egg retention shows a strong
correlation with brooding: 18 of 55 kn )wn brooding species (33 o/~)retain eggs, but
only 39 of 650 non brooding species (v,?~) have oviducal retention (Fisher's exact,
P < 10-5). In addition, live-bearing has arisen more frequently in brooding than in
non brooding genera: Live-bearing has evolved in eight of the IS brooding genera
containing more than one species (53 %), but in only 24 of the 150 polytypic nonbrooding genera (16,?~).The difference in proportions is significant (Fisher's exact,
P < .005).
We must be cautious that brooding species are not disproportionately found in
cold environments, as this could account for part of the above correlations, We do
not know definitely if brooding is correlated with cold, but the data in table 2 (here)
916
THE AMERICAN
NATURALIST
and in figure 1 of Tinkle and Gibbons (1977) suggest not. This possible bias can be
circumvented, however, by restricting the comparison to taxa in cold climates. Of 13
brooding genera with taxa in cold climates, live-bearing has arisen in 7 of these
(54 ~{»),whereas live-bearing has arisen in only 23 %of the non brooding genera found
in cold climates (23 of 101 genera; table 3 has only approximations of these data). If
we assume that the brooding and nonbrooding genera have had the same number of
species in cold climates (equal opportunity for the origin of live-bearing), then the
correlation is significant (Fisher's exact, P < .05). Therefore, it seems that brooding
enhances the evolution of live-bearing as well as the evolution of egg retention.
3. Egg retention and live-bearing should not evolve in response to aquatic or arboreal
life, or to extremes of soil moisture.-If these habitats promoted the evolution of
live-bearing, they should contain many species with egg retention and many livebearing species with egg-laying congeners. Table 3 does not support this prediction.
Species in these habitats have evolved egg retention and live-bearing about as often
as would be expected from their proportions in squamates as a whole (P> .05 in
all cases).
DISCUSSION
Live-bearing has evolved from egg-laying more than 30 times in squamate reptiles.
Several hypotheses have been presented here to account for the origin of live-bearing.
The model we advocate assumes that live-bearing evolves from egg laying only if the
intermediate stages of egg retention are selected for. Egg retention is a state in which
females delay laying and carry the eggs to allow partial embryonic development in
utero. If selection favors increasingly longer periods of egg retention, eventually the
population will ~ontain females which give birth to live young. This model is not
unique to our paper, but we have extended it as well as tested it.
Both theory and data suggest that two factors, cold environments and maternal
care of eggs, independently select for egg retention. Of these only cold climate seems
to favor the full transition to live-bearing; brooding merely facilitates the transition.
Cold climate has often been proposed as a major factor favoring the evolution of
live-bearing (Mell 1929; Weekes 1935; Sergeev 1940: Packard 1966: Greer 1966;
Packard et al. 1977). Sergeev even contended that cold climate was the single major
force in the evolution of squamate live-bearing, although he did not rule out all other
ecological factors (e.g., aquatic habitats), merely regarding them as having small
overall effects. This study supports Sergeev's contention that cold is the major force,
but his case can perhaps be made more strongly, because origins of live-bearing
outside of cold environments seem to be rare. A demonstrative case is provided by
brooding. which readily leads to egg retention. If many factors even weakly selected
for live-bearing, then we would expect brooding to enhance this selection so that at
least some origins of live-bearing would not occur ~ncold climates. Yet, at least six of
the eight recent origins of live-bearing in brooding genera have been in cold climates,
and perhaps all of them are (one genus unknown, one-half the examples of another
genus inhabit cold climates).
We have emphasized two somewhat different reasons why cold may be important
EVOLUTION
OF LIVE-BEARING
917
in the evolution of live-bearing: (a) Cold may injure the embryos at the time of
laying; (b) cold may slow development so that hatching occurs later than is optimal.
Hypothesis (a) requires that ground temperatures at the time of ovulation must be
Iow enough to harm the embryos. This is directly testable on a species-by-species
basis, but there is no universal temperature minimum which can be considered
injuriously cold. Ground temperatures which are lethal to eggs of a tropical species
may be warm by temperate standards. For example, eggs of a tropical iguana, which
develop normally at 30° C, cannot tolerate even a week's exposure to 20° C (Licht
and Moberly 1965). Twenty degrees C is not lethal to eggs of some temperate species
(Sergeev 1940). Hypothesis (b) is very general because it argues an advantage for egg
retention whenever the ground is cooler than the mother and the young benefit by
earlier hatching. Early hatching could be advantageous for various reasons in
seasonal environments, such as seasonal food availability or the approach of winter
(Packard et al. 1977). Such generality might limit the usefulness of the cold climate
hypothesis (b) were it not for a qualification. The cost of retaining eggs is likely to be
proportional to the duration of retention, whereas the benefit depends upon how
much the offspring's development is accelerated. A long duration of retention will
have little effect on development time if the ground is only slightly cooler than the
mother. Thus, environments which are cold by other standards (harmful to embryogenesis) are the ones likely to provide the most benefit from egg retention.
There is one critical test of the above cold-climate hypotheses that may be feasible.
Hypotheses (a) and (b) cannot explain egg retention in a female that lays several
clutches per season, unless it is only the first and/or last clutch that is retained. If egg
retention is found in such a female, then there is likely a nonthermoregulatory basis
for its evolution. "'
The strong correlation between cold climate and origin of live-bearing does not
indicate that we have anticipated the correct reason for the correlation. Although we
and others have suggested that cold climate is the evolutionary cause oflive-bearing,
it could be that cold climate merely correlates with some other factor that is a more
direct cause of live-bearing or that cold climate is indeed the cause but that we have
misinterpreted how it selects for live-bearing. For example, Tinkle and Gibbons
(1977) suggest that the evolution of live-bearing in cold environments may not have a
thermoregulatory basis. Instead they suggest that cold climates (i) are variable, so
that eggs in a nest face many unpredictable sources of mortality, and (ii) lengthen
development. thus exposing the eggs to even more sources of mortality than
otherwise. In the Tinkle and Gibbons model, retention evolves to shorten the interval
in the nest, not necessarily to shorten the total incubation time. Further elucidation
of these alternative hypotheses requires detailed studies on species with egg retention,
but at present there is circumstantial evidence in favor of the thermoregulatory
hypothesis (h) for three species, Lacerta muralis, L. viridis (Cooper 1965), and Natrix
"at,.i" (Smith 1973). All three species show the intermediate stages of egg retention
and all inhabit environments so cold that there is insufficient time to permit
spring-laid eggs to hatch before winter. Natrix natrix not only shows lengthy egg
retention. but also nests in compost heaps, the warmest available microhabitat.
Despite this, eggs do not hatch before winter if the summer is cold (Smith 1973).
918
THE AMERICAN NATURALIST
SUMMARY
Most reptiles lay eggs, but many lizards and snakes give birth to live young by
retaining the eggs within the oviducts until birth. The origin of live-bearing in reptiles
is investigated here by posing a theoretical model and te.l>tingthe model with
published data. Predictions are (1) that live-bearing should evolve in cold environments and (2) that maternal care of the eggs facilitates the evolution of live-bearing.
Analyses of data from over 1,000species of lizards and snakes reveal that live-bearing
has evolved recently at least 38 times, and an additional 60 species show the
intermediate evolutionary stages (egg retention). Tests of these data support the
predictions: Species which have recently evolved live-bearing or show the intermediate stages are much more likely to be found in cold climates or have maternal
care of eggs than are squamates in general. The presentation in this paper differs from
those of most earlier workers in distinguishing the cases in which live-bearing arises
from the cases in which a live-bearing species radiates and invades new habitats.
ACKNOWLEDGMENTS
We dedicate this paper to Henry S. Fitch (University of Kansas). Without his
pioneering work on reptilian life histories, and particularly his 1970 review of
squamate reproduction. the present study would not have been feasible.
Raissa L. Berg (University of Wisconsin) kindly translated the paper by Sergeev
(1940) from Russian to English. We thank Donald W. Tinkle for encouragement,
useful suggcstions on an earlier manuscript, and for a copy of an unpublished
manuscript. We are also grateful to H. S. Fitch, O. Cuellar, E. L. Charnov. G. H.
Pykc, J. M~'Legler, G. C. Packard, S. N. Salt he. A. E. Greer, and J. H. Werren for
their comments. We gratefully acknowledge the support of a University of Utah
Posdoctoral Fellowship (to RS) and a University of Utah Research Fellowship (to
.18). We thank Toni Kinser for typing the manuscript.
APPENDIX
THE EVOLUTION OF EGG RETENTION
It is useful to consider a model which incorporates changes in fecundity and survival to
understand how selection acts on the evolution of egg retention. Since this paper deals with
reptiles, the model incorporates assumptions which approximate the natural history of
reptiles: overlapping generations with reproduction at regular intervals. Each reproduction is
limited to one clutch of eggs, and we further assume that adult survival and fecundity are
independent of age. The average fecundity of a female in such a population can be represented
by the series
Ra
= sb +
_
2
sb
spb + sp b + .. . = I -,
-p
(AI)
in which s is juvenile survival from laying to first reproduction, b is fecundity in daughters, and
p is adult survival from one reproduction to the next (e.g., Wilson and Bossert 1971). In a
population constant in number, fecundity (Ro) is a measure of fitness, and it can be shown that
a rarc dominant gene which increases Ro in females (having no effect on sex ratio or male
fertility) will increase in frequency (technique in Charnov 1979). Thus, we have the intuitive
result that selection in a stable population favors a gene which increases fecundity. In the
EVOLUTION
OF LIVE-BEARING
notation of (AI), fecundity increases if
s'b'
->l-p'l-p'
sb
, b'
s li>s
919
or
1- p'
I-p'
(A2)
with primes indicating the parameters of the rare type.
Result (A2) is at least qualitatively applicable to the evolution of egg retention. In the text
we suggest that the general effect of egg retention is to lower fecundity and adult survival.
Thus, we often expect b'jb < 1 < (I - p')j(1 - p). Under these conditions, egg retention is
most likely to evolve if egg survival s' is much greater than s. If however, b'jb,
(I - p')j(1 - p) ~ 1, then s need not increase greatly, and egg retention is again likely to
evolve. We look for the ecological conditions tending toward either extreme of s' ~ s or b'jb,
(I - p')j(1 - p) ~ 1.
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