The origin of evolutionary innovations ... - Wiley Online Library

Functional Ecology 2008, 22, 317–322

doi: 10.1111/j.1365-2435.2007.01359.x

The origin of evolutionary innovations: locomotor consequences of tail shape in aquatic snakes

Blackwell Publishing Ltd

F. Aubret* and R. Shine School of Biological Sciences A08, University of Sydney, NSW 2006, Australia

Summary 1. Phylogenetic shifts in habitat use often impose strong selective forces on locomotor systems; for example, the transition from terrestrial to aquatic existence has stimulated the evolution of laterally compressed ‘paddles’ on the tails, feet or fins of a diverse array of vertebrate taxa. 2. Under the traditional gradualist model of evolutionary change, even a small paddle is predicted to enhance aquatic locomotion but impose a cost in terrestrial performance. However, direct evaluation of those early evolutionary stages is impossible from modern-day aquatic species, because the initial steps have been obscured by complex subsequent adaptations of morphology, physiology and behaviour. 3. Unlike most major features of locomotor-system morphology (e.g. leg length, muscle mass), the caudal paddles of aquatic snakes are morphologically so simple that they can be recreated experimentally. We attached artificial paddles to the tails of juvenile tigersnakes (Notechis scutatus) to assess the effect of tail shape on locomotor performances. 4. The presence of a small paddle on the tail greatly increased swimming speeds (by 25%) but decreased crawling speeds on land (by 17%). A small paddle (35% of tail length) was more effective for aquatic locomotion than a larger paddle (84% of tail length). 5. Presumably, larger paddles are effective only after adaptive modification of musculoskeletal propulsive systems. Our experimental manipulations thus provide unusually direct evidence of a functional advantage to modest lateral flattening of the tail in the earliest aquatic snakes, mediated via enhanced locomotor speeds in water. Key-words: aquatic locomotion, evolutionary transition, Notechis, paddle, snake

doi: 10.1111/j.1365-2435.2007.0@@@@.x Functional Ecology (2007) xx, 000–000

Introduction To identify the selective forces that have generated morphological and physiological diversity, functional morphologists examine relationships between an organism’s structure and its performance (Gans 1974, 1975, 1986). Links between morphology and locomotor performance have attracted particular attention in this respect because locomotor speeds are easier to quantify than are many other organismal functions (Bamstedt & Martinussen 2000; Brown et al. 2005; Lika & Papandroulakis 2005). Also, specific features of the locomotor system that enhance performance are sensitive to details of local environments; for example, a limb structure that enhances terrestrial speed may be poorly-suited to arboreal locomotion (Losos et al. 2000). Overall, locomotor systems generally function well in the circumstances in which they are usually employed (Losos 1990; Wainwright & Reilly 1994). This pattern is particularly *Correspondence author. E-mail: [email protected]

striking in lineages that incorporate a phylogenetic transition from one habitat type to another, with correspondingly abrupt shifts in the selective forces operating on locomotor systems. For example, the transition from terrestrial to aquatic life massively alters locomotor modes. Moving rapidly through a dense medium such as water (rather than through air) requires dramatic modifications of body shape, and of the ways in which propulsive forces are delivered (Fish 1996). Modern-day aquatic species thus share distinctive features including general body shape (lateral or vertical compression) and flattened structures that push against the water (e.g. fins, paddle-like tails), as well as a myriad of less obvious adaptations (Gingerich et al. 1994; Thewissen, Hussain & Arif 1994; Berta & Sumich 1999; Reynolds & Rommel 1999). This tight match between environmental challenge and locomotor system provides clear evidence of adaptation, but the functional significance of specific components of those systems remain unclear. In particular, what was the role of any such feature early in the adaptive process, when ancestrally terrestrial species first began exploiting aquatic habitats?

© 2007 The Authors. Journal compilation © 2007 British Ecological Society

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Fig. 1. Young tigersnakes were tested for locomotor performance under five conditions, from top to bottom: large paddle, small paddle, no paddle, long taping and short taping. The paddles were made of two pieces of electrical tape, cut into shape and taped together vertically, sandwiching the snake’s tail. The controls consisted of the same electrical tape, surrounding the tail but without enlarging the surface area. Bottom photograph shows the typical flattened tail of a sea-snake (Laticauda colubrina; photo X. Bonnet).

Modern-day aquatic species have accumulated adaptive modifications of many systems, so that it is not possible to isolate the effects of any single trait. For example, previous studies suggest that the flattened paddle-like tail of a sea-snake is a major reason why these animals can swim more rapidly than their terrestrial counterparts, but are slower on land (e.g. Shine & Shetty 2001a; Shine et al. 2003). However, the enhanced swimming ability of sea-snakes instead might be due to other morphological and physiological modifications (Heatwole 1999). Also, flattened tails might be effective for swimming only when they are fully developed, and thus the initial flattening of the tail might have been due to sexual selection (Shine et al. 1999; Shine & Shetty 2001b) or have been skipped through macromutation (Goldschmidt 1940). To demonstrate an adaptive origin for such a trait, we need to find (or create) an organism identical to the terrestrial ancestor in all respects except for that trait. Only then can we test predictions about the nature and magnitude of performance effects. For example, the case of the sea-snake’s paddle-like tail would lead us to predict that a terrestrial snake with such a tail shape would swim faster but crawl more slowly than a counterpart with a normally tapering tail. Additionally,

gradualist theory would predict that even a small paddle would enhance swimming success, and indeed in the initial stages of adaptation, a small paddle may be more effective than a larger paddle because the muscular strength and skeletal supports needed to overcome the water resistance of a large paddle would develop only later in the adaptive shift from land to the oceans. Although we could make similar predictions about any morphological feature putatively adaptive to a specific habitat type, the paddle-shaped tails of sea-snakes offer an unusual opportunity to test such ideas. Most morphological adaptations to specific habitats are so complex (e.g. limb size and shape, digit morphology: Howell 1970; Swartz 1998; Bejder & Hall 2002), and so closely integrated with other parts of the organism’s phenotype, that we cannot recreate a novel organism that differs from the ancestral form only in the trait of interest. However, apart from its lateral compression, the tail of a sea snake is comparable to the tapered tail of its terrestrial counterpart (Fig. 1). A swimming snake moves forward by accelerating portions of the surrounding water; the reaction to this effect generates the propulsive forces (Gans 1973, 1975). Thus, by placing a piece of electrical tape on either side of the tail, we can simulate the vertical flattening seen in sea-snakes, and substantially increase the amount of water which the tail-tip displaces as it arcs from side to side during swimming. To see whether this artificial ‘flattening’ of the tail affects the speed of swimming snakes, we conducted trials with a terrestrial snake species from a lineage that gave rise to sea-snakes (Keogh 1998), to clarify the functional significance of tail-flattening during the early stages of the invasion of the oceans by terrestrial snakes.

Materials and methods STUDY SPECIES

Tigersnakes (Notechis scutatus, Elapidae) are large and highly venomous front-fanged terrestrial snakes that are widely distributed through coastal regions of southern and eastern Australia (Cogger 1992). This species may be relatively close to the lineage that gave rise to the hydrophiine sea-snakes (Keogh 1998). Although primarily terrestrial, mainland tigersnakes are abundant in riparian habitats, and frequently enter the water to forage or to escape from predators (Mirtschin & Davis 1992).

STUDY SPECIMENS

For the main part of this study we used 16 young tigersnakes (7-months-old) born in captivity in April 2006. They were randomly selected from three litters (six, five and five snakes) obtained from pregnant females captured on Carnac Island (32°07′17″S; 115°39′43″E; 12 km off the coast of Fremantle, Western Australia) in March 2006. Although there is no permanent water on the island, Carnac Island tigersnakes are excellent swimmers (Aubret 2004). We kept the young snakes in a controlled temperature room (ambient temperature was 27 °C by day and 17 °C at night) in individual plastic cages (30 × 20 × 10 cm). At the time of testing the snakes averaged 12·79 ± 1·74 g in body mass (range: 10·60 –16·10 g), 34·01 ± 1·19 cm in total length (range: 31·70 – 36·00 cm) and

© 2007 The Authors. Journal compilation © 2007 British Ecological Society, Functional Ecology, 22, 317–322

Tail shape and swimming in snakes 319 28·56 ± 0·97 cm in snout-vent length (range: 26·50 – 30·0 cm) and 5·46 ± 0·27 cm in tail length (range: 5·00 – 6·00 cm).

EXPERIMENTAL DESIGN

We tested each snake for swimming and crawling performance under three conditions: no paddle, small paddle and large paddle. Each snake was tested only once per day (in the late morning) to avoid fatigue, and never within 7 days of feeding (to ensure an empty stomach). Testing and treatment order were balanced among snakes to avoid any effect of experience on swimming or crawling performance (i.e. half started with crawling tests; half with swimming tests; a third of each started under each of the three conditions described above).

Swimming speed We used a swimming track (225 × 35 × 38 cm) filled with water held at 27 °C (depth: 10 cm). The bottom of the pond liner was painted with a white (non-toxic) paint and line markers drawn every 30 cm. Snakes were dropped at one end of the track and were kept swimming back and forth the full length of the pool. To ensure maximal speed, we frequently tapped their tails with a stick. Velocity was calculated as time (in seconds) to traverse 30 cm sections of the track. Snakes were raced over a total distance of about 20 m, so that we were able to calculate 10 velocity estimates per individual per treatment. For each snake, we also calculated stride length (the distance swum in one complete undulation cycle; calculated over cycles of 3–8 successive undulations), undulation frequency and tail-beat amplitude under the three conditions (no paddle, small or large paddle).

and reduces swimming performance in tadpoles (Wassersug & Hoff 1985). To simulate vertical flattening of the tail as seen in sea-snakes, we placed a piece of electrical tape on either side of the tail to increase the amount of water which the tail-tip displaced as it arced from side to side during swimming. The artificial paddles were made from two pieces of electrical tape, cut into a paddle shape with scissors and then taped together vertically, sandwiching the snake’s tail (see Fig. 1).

CONTROLS

The application of electrical tape to a snake’s tail may alter its swimming performance regardless of any ‘paddle’; for example, due to stiffening of the tail. To examine this possibility, we used another 15 4-month-old tigersnakes randomly selected from four different litters (five, five, three and two snakes). They were born in March 2007 to four pregnant females captured beside Lake Joondalup in Western Australia (31°45′12″S; 115°47′38″E) in February 2007. There is minimal divergence between mainland WA and Carnac Island tigersnakes in genetic traits (< 0·3%; Keogh, Scott & Hayes 2005) or swimming ability (Aubret 2004). Swimming performance was recorded as described above. We used three treatments for each snake: no taping, short taping (distal third of the tail) and long taping (distal three-fourths of the tail). Tape was applied to the tail, surrounding it but without increasing the surface area (see Fig. 1). At the time of testing snakes averaged 8·17 ± 1·05 g in body mass (range: 6·40 –10·60 g), 25·90 ± 1·77 cm in total length (range: 22·80–29·00 cm) and 21·99 ± 1·44 cm in snout-vent length (range: 19·50 – 24·50 cm) and 3·91 ± 0·45 cm in tail length (range: 3 – 4·60 cm). In both experiments, there was no noticeable change in snake behaviour while swimming or crawling due to the application of tape on the tail.

Crawling speed We recorded the speeds at which snakes crawled (via lateral undulation) along a 1-m long track made of a PVC half-pipe, with Attapulgite (clay) as substratum. Attapulgite is a natural dry stone with a gravel-like texture, enabling us to measure snake locomotion in a standardized and repeatable way. Trials were video taped and the speed repeatedly recorded over two 30 cm section of the pipe. Unlike swimming trials, crawling trials often elicited defensive behaviour from the young tigersnakes. In consequence, we could not record speeds over successive lengths, because in many cases the snakes reversed direction to display to the observer. To ensure maximal speed, we stimulated the snake by touching its tail with a paint brush. For each treatment (no paddle, small or large paddle) approximately 10 lengths were recorded. Each snake was tested twice on different days and the fastest performance retained for analysis.

ADDITION OF ARTIFICIAL PADDLES

A swimming snake moves forward by accelerating portions of the surrounding water, thus generating propulsive forces (Gans 1973, 1975). Jayne & Bennett (1989) found that natural tail loss had no effect on terrestrial locomotion in a population of land snakes (i.e. with a normal slender tail), and experimental tail removal suggested that tail length was relatively unimportant until over half of the tail was lost. In the case of aquatic locomotion, however, tail loss reduced burst swimming speed in adult tigersnakes (Aubret, Bonnet & Maumelat 2005). Moreover, the loss of the tip of the tail, although not actively involved in the production of thrust, alters waveform

DATA ANALYSES

All locomotor trials were video taped (JVC hard disk camcorder; 25 frames per second) and digitally processed on a laptop computer. Data were log-transformed prior to analysis.

Results SWIMMING

The small and large paddles differed in percentage of the tail length covered (respectively, 35·1 ± 4·3 vs. 84·1 ± 11·4%;  F1,29 = 242·59; P < 0·0001), surface area of the paddle (134·1 ± 17·5 vs. 536·2 ± 71·23 mm2, F1,29 = 451·32; P < 0·0001), and paddle mass as percentage of snake body mass (0·30 ± 0·06 vs. 1·38 ± 0·25%, F1,29 = 241·99; P < 0·0001). Swimming speeds of the young snakes were strongly affected by our treatments (repeated measures design, Wilk’s λ = 0·32; P < 0·0001; Fig. 2). Snakes swam about 25% faster after we attached small paddles to their tails, compared to their speeds without paddles, or with large paddles. This effect was evident in mean swimming speeds (respectively, 49·25 ± 5·78 vs. 39·71 ± 4·23 vs. 42·27 ± 6·26 cm s–1; effect of paddle F2,45 = 12·92; P < 0·00001) as well as maximum swimming speeds (see Fig. 3). Unsurprisingly, maximum swimming speeds decreased during any given trial as the snakes became tired (effect of time F9,405 = 18·18; P < 0·0001), and this decrease occurred at


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Fig. 2. Sixteen young tigersnakes were video taped swimming along 10 successive lengths of a track, under three conditions: no paddle (black triangle), small paddle (open circle) and large paddle (grey square; see text for details). Swimming speeds of the young snakes were strongly affected by our treatments (repeated measures design, Wilk’s λ = 0·32; P < 0·0001). Snakes swam about 25% faster after we attached small paddles to their tails, compared to their speeds without paddles, or with large paddles. Means ± SE are plotted.

Fig. 4. Fifteen young tigersnakes were videotaped swimming along 10 successive lengths of a track, under three conditions: no tape (black triangle), short taping (open circle) and long taping of the tail (grey square). There was little overall effect of taping on swimming performance (see text for details).

CRAWLING

Our treatments also affected terrestrial speeds: snakes crawled 17% faster when unencumbered (no paddle) than when fitted with either small or large paddles (see Fig. 3).

CONTROLS

Fig. 3. Snakes swam about 25% faster after we attached small paddles to their tails, compared to their speeds without paddles, or with large paddles (65·35 ± 7·71 vs. 51·15 ± 5·33 vs. 56·12 ± 6·74 cm s–1; F2,45 = 18·66; P < 0·0001). On the other hand, snakes crawled about 17% faster when unencumbered (no paddle) than when fitted with either small or large paddles. Burst crawling speed averaged 37·14 ± 5·96 cm s–1 with no paddle attached, vs. 30·49 ± 5·15 cm s–1 with the small paddle attached and 30·50 ± 6·60 cm s–1 with the large paddle attached (F2,42 = 6·30; P < 0·0041).

similar rates regardless of treatment (interaction F18,405 = 1·36; P = 0·15; see Fig. 2). Locomotor kinematics were also affected. Stride length was greater during swimming trials with a small paddle (126·06 ± 13·90 mm) than with a large paddle (105·22 ± 25·12 mm) or no paddle (110·37 ± 17·27 mm; F2,45 = 4·87; P < 0·012). Undulation frequency was similar (respectively, 4·90 ± 0·81; 4·47 ± 1·04; and 4·22 ± 0·54 undulations per second; F2,45 = 2·56; P = 0·089) and tail-beat amplitude differed only slightly between the three treatments (respectively, 37·45 ± 11·46 vs. 44·23 ± 6·83 vs. 47·45 ± 12·77 mm; F2,45 = 4·60; P < 0·015).

Taping length averaged 35·91 ± 4·55% of tail length (short taping) vs. 82·87 ± 5·19% (long taping;  F1,27 = 625·53; P < 0·0001), similar to the lengths used for short and long paddles in the main experiment (both P > 0·47). Taping a large area of the tail significantly affected swimming speed (repeated measures design, Wilk’s λ = 0·55; P = 0·32; interaction term F18,378 = 1·98; P < 0·010), by delaying the initial acceleration over the four first lengths of the track (see Fig. 4). There was however no difference in mean swimming speeds between the control, large taping and small taping treatments (respectively, 37·48 ± 4·65 vs. 36·18 ± 4·75 vs. 37·73 ± 6·13 cm s–1; F2,42 = 0·33; P = 0·72), nor in maximum swimming speeds (50·22 ± 8·23 vs. 45·98 ± 5·59 vs. 49·85 ± 6·85 cm s–1; F2,42 = 1·41; P = 0·26). Restricting the analysis to the first four lengths swum, the long taping induced a 11·4% decrease in average swimming speed compared to the two other treatment groups, but the difference fell short of statistical significance (F2,42 = 3·13; P = 0·055). A short length of tape on the tail had no detectable effect on swimming performance (compared to the untaped snakes, all P > 0·56).

Discussion Our experimental data show that lateral compression of the tail enhances aquatic speed but retards terrestrial speed in young tigersnakes. The extent to which a small artificial paddle enhanced swimming speed was surprising: a 25% increase in speed, 14% increase in stride length and 21% decrease in tail-beat amplitude compared to snakes without a paddle. A large paddle however had little effect on swimming, except for a slight (5%) decrease in stride length.


Tail shape and swimming in snakes 321 Why isn’t a larger paddle more effective than a smaller one? The stiffening effect of the tape on the tail, or perhaps increased drag, may partly explain this effect but cannot be the only reasons. The proportion of the tail covered by the small artificial paddle (5·56 ± 0·65% of body length) was much less than that involved in the naturally flattened tails of sea snakes (e.g. Pelamis platurus –11·2 ± 0·7%; Graham et al. 1987). However, the long artificial paddle was of similar size (13·46 ± 1·76% of body length) to natural sea-snake paddles. A small paddle proved more effective than a large one in accelerating swimming, although the ‘cost’ to terrestrial locomotion was similar for the two sizes of paddle. In keeping with the gradualist paradigm (Darwin 1859; Fisher 1930), this result suggests that over evolutionary time the flattened area of the tail may have increased concurrently with modification of other features that facilitate aquatic propulsion, for example, components of the musculoskeletal apparatus. Thus, whether or not selection would favour flattening of the tail in ancestral amphibious snakes presumably would depend upon the magnitude of fitness differentials arising from locomotor speeds in water vs. on land. That is, are the benefits of faster swimming great enough to offset the costs of slower crawling? The answer to that question depends upon the amount of time that the animals spend in each medium, and the frequency with which fitness-relevant events (feeding, mating, escape from predation) occur in water vs. on land. It is easy to imagine a scenario whereby aquatic locomotor advantages outweigh terrestrial locomotor disadvantages, allowing gradual evolution of a paddle-like tail. Contrariwise, caudal flattening would decrease not increase fitness in most terrestrial environments, and thus would not be favoured. Presumably for this reason, most semi-aquatic snakes exhibit ‘normal’ (slender, tapering) tails (i.e. Natrix, Nerodia, Boulengerina, Eunectes). In at least one entirely aquatic lineage (the filesnakes or Acrochordidae), the tail also retains its ancestral (tapering) shape but loose skin on the body flattens to form a large paddle during swimming (Shine & Houston 1993). Both swimming and crawling trials suggest that tail shape may be under strong stabilising selection in snakes, with even minor changes conferring strong costs in the ‘wrong’ environment. This hypothesis is supported by reports of fitness differentials associated with tail length and width in other snakes including sea snakes (Shine et al. 1999; Shine & Shetty 2001b). The magnitude of locomotor effects recorded in our study also accords with the ubiquity of paddle evolution in purely aquatic animals. Many animals requiring dynamic movement through water have evolved adaptations such as paddles, fins or webbed appendages, with examples spanning a wide array of taxa including mammals, fishes, birds, reptiles, amphibians and arthropods (Maddock, Bone & Rayner 1994). Understanding the selective forces involved in major evolutionary transitions (such as from terrestrial mammals to aquatic whales, or from small carnivorous mammals to flying bats) will always be a difficult challenge. Although much can be inferred from fossils, functional consequences of morphological variation are difficult to assess with such

fragmentary evidence. Similarly, current-day representatives of these lineages exhibit complex and inter-related adaptations to life in the ‘new’ environment, and thus can tell us relatively little about the ancestral selective pressures that acted on the evolution of new locomotor features. The transition from terrestrial to aquatic life in snakes offers a powerful model system to ask such questions, because the simplified body plan of these animals allows us to physically recreate potential intermediate stages between fully terrestrial and fully aquatic organisms (cf. Shine 2002). We can then examine issues such as the predicted locomotor trade-offs between morphological adaptations to aquatic vs. terrestrial locomotion. Our results provide strong empirical support for the plausibility of gradual evolution of the novel morphological features that ultimately were critical to major evolutionary transitions.

Acknowledgements We thank S. Simpson and J. K. Webb for discussions on predatory behaviour in aquatic vertebrates. The Department of Environment and Conservation (Western Australia; permits #SF005274 and #CE001216), supported the study. The Animal Ethics Committee (University of Sydney) approved all procedures (Project L04/3-2006/4297). Funding was provided by the Australian Research Council. We also wish to thank Jai Thomas, Melanie Elphick, and Radika Aubret for important help at various stages of the preparation of this manuscript. John Weigel and Craig Adams provided crucial advice on snake husbandry. Zoé Lechat helped with videotaping and editing locomotor trials. Several anonymous referees provided many useful suggestions that improved this manuscript.

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