Evidence for a receiver bias underlying female preference for a male mating pheromone in sea lamprey

T J Buchinger; H Wang; W Li; N S Johnson

doi:10.1098/rspb.2013.1966

. 2013 Nov 22;280(1771):20131966. doi: 10.1098/rspb.2013.1966

Evidence for a receiver bias underlying female preference for a male mating pheromone in sea lamprey

T J Buchinger ¹, H Wang ¹, W Li ¹, N S Johnson ^2,^✉

PMCID: PMC3790490 PMID: 24068361

Abstract

Receiver bias models suggest that a male sexual signal became exaggerated to match a pre-existing sensory, perceptual or cognitive disposition of the female. Accordingly, these models predict that females of related taxa possessing the ancestral state of signalling evolved preference for the male trait in a non-sexual context. We postulated that female preference for the male-released bile alcohol mating pheromone, 3 keto petromyzonol sulfate (3kPZS), of the sea lamprey (Petromyzon marinus) evolved as a result of a receiver bias. In particular, we propose that migratory silver lamprey (Ichthyomyzon unicuspis), a basal member of the Petromyzontidae, evolved a preference for 3kPZS released by stream-resident larvae as a means of identifying productive habitat for offspring. Larval silver lamprey released 3kPZS at rates sufficient to be detected by migratory lampreys. Females responded to 3kPZS by exhibiting upstream movement behaviours relevant in a migratory context, but did not exhibit proximate behaviours important to mate search and spawning. Male silver lamprey did not release 3kPZS at rates sufficient to be detected by females in natural high-volume stream environments. We infer that female silver lamprey cue onto 3kPZS excreted by stream-resident larvae as a mechanism to locate habitat conducive to offspring survival and that males do not signal with 3kPZS. We suggest that this female preference for a male signal in a non-sexual context represents a bias leading to the sexual signalling observed in sea lamprey.

Keywords: receiver bias, cyclostomata, lamprey, communication, 3kPZS, mate choice

1. Introduction

Biologists have long been fascinated by natural complements, especially concerning the evolution of matching pairs (i.e. receptor and ligand [1]). Such questions are particularly interesting in understanding the origins of sexual communication systems, where the pair of interest is often female preference and male signal. Classical sexual selection models (i.e. Fisher's runaway, indirect/direct benefits) suggest that female preference and male signalling have coevolved [2]. Receiver bias models are an alternative suggesting that the male trait involved in sexual signalling exploits a bias in the sensory system of the female [3], stemming from either female perception or cognition of a trait. A perceptual bias results when a particular trait is inherently stimulatory of the female's sensory system (sensory exploitation [4,5]). Cognitive biases occur when female preference for a trait evolves in a non-sexual context (sensory trap [6]). Some of the strongest support for the receiver bias hypothesis comes from the nuptial colours of the guppy (Poecilia reticulata [7]) and the stickleback (Gasterosteus aculeatus [8]), the courtship behaviours of watermites (Neumania papillator [9,10]), and the mating calls of frogs (Physalaemus pustulosus [5]), each of which presents a clear biological function of the behaviours creating biases in the females sensory system [11].

The influence of biases in the female sensory system on chemical mating signals has been suggested, but not empirically tested, as have auditory [5], visual [7,8] and tactile [10] sensory modalities. The identification of male insect pheromones as floral compounds has led to hypotheses of the involvement of receiver bias in the evolution of female preferences [12,13]. Research into fish chemoreception has resulted in similar hypotheses of the origin of odour preferences [14], where sex steroids [15], prostaglandins [16], amino acids [17] and bile salts [18] are detected with acute sensitivity and specificity, and influence receiver behaviour. In many cases such odour preferences probably represent fish cueing onto the unspecialized release of a compound [14,19]; however, some fish appear to be signalling to the receiver [20,21]. One example of the use of a specialized mating pheromone is that of the sea lamprey (Petromyzon marinus [18]).

The sea lamprey is a jawless vertebrate that relies upon olfaction to complete the final stages of its semelparous life [22]. Conspecific odours facilitating the migration of reproductive adults and the subsequent spawning act have been of particular interest [23,24]. Bile salts and derivatives excreted by stream-resident larvae are hypothesized to direct adults from lakes or the Atlantic Ocean into streams with a recent history of high offspring survival [25,26]. Upon sexual maturation, males release at exaggerated rates (approx. 0.5 mg h⁻¹) 7α, 12α, 24-trihydroxy-5α-cholan-3-one-24-sulfate (3 keto petromyzonol sulfate, 3kPZS), a bile alcohol which induces long-distance upstream movement and near-source behaviours in sexually mature females [18,27,28,29].

In general, the involvement of a sensory trap in the origin of a preference/signal pair is supported by two lines of evidence: (i) the shaping of female preference by natural selection, rather than sexual selection; and (ii) the origin of female preference prior to the appearance of the male trait that exploits the preference [9,10]. Here, we provide evidence for a sensory trap in the origin of the sea lamprey mating pheromone by demonstrating that female preference for 3kPZS in a basal member of the Petromyzontidae, the silver lamprey (Ichthyomyzon unicuspis) [30–35], evolved in a non-sexual context, and that the preference has not been exploited by males.

2. Material and methods

(a). Experimental animals

Experimental lampreys were used with approval from Michigan State University's Animal Use and Care Committee (Approval no. 04/10-043-00). Larvae were collected via backpack electroshocking, and adults were caught in United States Fish and Wildlife Service sea lamprey traps. Lampreys were transported to Hammond Bay Biological Station, Millersburg, Michigan, where larvae were immediately used in experiments and adults were stored in 4°C 1000 l flow-through tanks. Adult females were distinguished from males based on a large, soft abdomen. Sexual maturity was determined based on the expression of eggs (ovulation) or milt (spermiation) with gentle manual pressure [27]. All sample collection and behavioural assays were conducted between sunset and sunrise due to the nocturnal behaviour of lampreys.

(b). Release of 3kPZS

Larval release of 3kPZS was investigated following methods similar to those used in the collection of sea lamprey larval odours [36]. However, release experiments were conducted immediately following collection, due to concerns of potential changes in bile alcohol release resulting from artificial holding and feeding. Larvae (weight = 2.33 ± 0.12 g, length = 109.4 ± 1.71 mm; mean ± s.e.) were sampled from Canada Creek, Montmorency County, Michigan, and Black River, Cheboygan County, Michigan, across the lamprey reproductive season (May–July, sampling events = 7). Approximately 30 larvae were collected within each sampling event, divided into three groups, and placed in a 5 l container with 10 cm of sand and aeration, supplied with ambient Lake Huron water. Following a 24 h acclimation period, the inflow of water was shut off, the lake-water decanted and 4 l deionized water added. The odour of larvae was allowed to accumulate for 12 h, after which a 1 l water sample was spiked with 5 ng 5-deuterated 3kPZS (5-d 3kPZS) [37,38] internal standard and stored at less than −20°C for later analysis. Previous experiments found minimal 3kPZS in water void of larvae (approx. 0.01 ng ml⁻¹). The bile alcohol 3α,7α,12α,24-tetrahydroxy-5α-cholan-24-sulfate (petromyzonol sulfate, PZS) was also quantified to allow for a comparison with previous reports of release rates by larval silver lamprey [39].

The 3kPZS released by adults was investigated by collecting holding waters (washings) from pre-ovulated (weight = 47.2 ± 0.64 g, length = 275.81 ± 1.51 mm; mean ± s.e.) and ovulated (weight = 58.22 ± 1.56 g, length = 277.1 ± 2.23 mm; mean ± s.e.) female, and pre-spermiating (weight = 43.83 ± 0.58 g, length = 281.06 ± 1.33 mm; mean ± s.e.) and spermiating (weight = 40.25 ± 0.37 g, length = 258.83 ± 0.76 mm; mean ± s.e.) male silver lamprey. Washings from spermiating male sea lamprey (weight = 236.75±4.44 g, length = 436.33±15.98 mm; mean±s.e.) were collected to provide a point of reference. A single individual was held in 5 l of aerated, deionized water. After 2 h, a 250 ml water sample was spiked with 5 ng 5-d 3kPZS and stored at less than −20°C for later analysis. A pair-wise Wilcoxon rank-sum test (α = 0.05) with a Holm adjustment for multiple comparisons [40] was used to evaluate differences in 3kPZS released by each sex, maturity and species.

A 10 ml subsample from each water sample was evaporated using a CentriVap Cold Trap with CentriVap Concentrator (Labconco, MO) and reconstituted in 50% HPLC-grade methanol. Concentrated samples were subjected to ultra-high-performance liquid chromatography with tandem mass spectrometry (UHPLC-MS/MS; Waters Acquity ultra-performance liquid chromatography system, Waters, Milford, MA; Micromass Quattro Premier XE tandem quadruple mass spectrometer, Waters, Manchester, UK) following described methods [37,38].

(c). Behavioural response to 3kPZS

(i). Two-choice maze

The near-source preference of pre-ovulated and ovulated female silver lamprey to 1 × 10^–12 M 3kPZS was determined using a two-choice maze [18] (figure 1a). The 3kPZS concentration used followed that of previous studies [29]. Briefly, a single silver lamprey was introduced to the furthest downstream point of the maze. After a 10 min acclimation, the time the silver lamprey spent in each channel was recorded by hand and by an infrared camera. After 20 min of recording, 3kPZS dissolved in 50% methanol (MeOH : H₂O, v : v) was introduced to a random side, along with a 50% methanol control vial to the opposing side. The odour was pumped into the maze for 5 min without recording the silver lamprey's behaviour. After 5 min, the behaviour was recorded for another 20 min. After recording the time spent in the control and experimental channels before odour application (bc, be), and the time spent in the control and experimental channels after odour application (ac, ae), an index of preference (i) was calculated for each test (i = [ae/(ae + be) − ac/(ac + bc)]). The indices of preference were evaluated using a Wilcoxon signed-rank test (α = 0.05) [18].

(ii). Quasi-natural stream

The response of pre-ovulated and ovulated female silver lamprey, and ovulated sea lamprey, to 1 × 10⁻¹² M 3kPZS was also evaluated in a quasi-natural stream system (figure 1b). Four passive integrated transponder (PIT) antennae were constructed to monitor the movement of lampreys (one upstream of the release cage, one downstream of the release cage and one at each of two nests constructed at the uppermost point of the system). At least 12 h prior to experimentation, two to five lampreys were implanted with 12 mm PIT tags (Oregon RFID, Portland, OR) and placed in an acclimation cage in the stream adjacent to the constructed system. Thirty minutes prior to experimentation, lampreys were moved from the acclimation cage to the release cage in the experimental system. The experiment began with the application of an odour into the designated channel. Fifteen minutes after odour application, lampreys were released from the acclimation cage and allowed to swim freely for 1 h. Movement of lampreys upstream of the release cage and the first choice of nest selection based upon odour application were evaluated as binary data using logistic regression [29]. Two treatments were applied to the channels: (i) 1 × 10⁻¹² M 3kPZS versus methanol and (ii) methanol versus methanol. Both the treatment (3kPZS or MeOH) and the channel activated with the treatment (left or right) were alternated and lampreys were only used once for each treatment. Logistic regression models showed no evidence of over-dispersion.

3. Results

(a). 3kPZS release

Release rates of 3kPZS and PZS by larval silver lamprey were 40.75 ± 8.8 ng larva⁻¹ h⁻¹ and 4.76 ± 1.85 ng larva⁻¹ h⁻¹, respectively (mean ± s.e.; figure 2; see electronic supplementary material). The recovery of 5d-3kPZS in larval washings was 69.12 ± 6.27% (mean ± s.e.). Analysis of adult lamprey holding waters showed differences in 3kPZS concentration between the sex, maturity and species combinations examined, whether standardized by weight (text below) or by individual (Wilcoxon rank-sum test, α = 0.05, Holm's adjustment; figure 3). Spermiating male sea lamprey released 3kPZS at the highest rate (212.7 ± 22.7 ng g⁻¹ h⁻¹, n = 8; mean ± s.e.), followed by spermiating and pre-spermiating male silver lamprey (5.05 ± 1.48 ng g⁻¹ h⁻¹, n = 23, and 1.16 ± 0.38 ng g⁻¹ h⁻¹, n = 17, respectively; mean ± s.e.), and pre-ovulated and ovulated female silver lamprey (0.41 ± 0.06 ng g⁻¹ h⁻¹, n = 16, and 0.12 ± 0.03 ng g⁻¹ h⁻¹, n = 9, respectively; mean ± s.e.). The recovery of 5d-3kPZS in adult washings was 59.19 ± 1.81% (mean ± s.e.). One outlier was removed from spermiating silver lamprey (1009.16 ng g⁻¹ h⁻¹) as it was approximately five standard deviations from the mean.

Figure 3. — Mean rate (ng adult⁻¹ h⁻¹) at which 3 keto petromyzonol sulfate (3kPZS) was released into the water, presented on a log scale. Letters represent significant differences as determined using a pair-wise Wilcoxon rank-sum test (α = 0.05) with a Holm adjustment for multiple comparisons. p-of sil, pre-ovulated female silver lamprey; of sil, ovulated female silver lamprey; p-sm sil, pre-spermiating male silver lamprey; sm sil, spermiating male silver lamprey; sm sl, spermiating male sea lamprey.

(b). Behavioural response of adult female silver lamprey to 3kPZS

The upstream movement of both pre-ovulated and ovulated female silver lamprey in the quasi-natural stream was influenced by 3kPZS, with a higher proportion of females moving upstream of the release cage when 3kPZS was applied than when methanol was applied (n : n = 30 : 25, 3kPZS = 11, MeOH = 3, χ² = 4.62, d.f. = 1, p = 0.032, and n : n = 15 : 13, 3kPZS = 14, MeOH = 1, χ² = 21.38, d.f. = 1, p ≤ 0.001, respectively; figure 4b). However, entry of pre-ovulated and ovulated female silver lamprey into 3kPZS-baited nests was not significantly different from that into methanol-baited nests (n = 30, 3kPZS = 4, MeOH = 2, χ² = 0.68, d.f. = 1, p = 0.41, and n = 15, 3kPZS = 8, MeOH = 4, χ² = 1.36, d.f. = 1, p = 0.24, respectively; figure 4a). Likewise, pre-ovulated and ovulated female silver lamprey showed no preference for 1 × 10⁻¹² M synthesized 3kPZS in two-choice maze experiments (Wilcoxon signed-rank test, p > 0.05; table 1). In the quasi-natural stream, ovulated female sea lamprey were attracted to the source of 3kPZS (n = 20, 3kPZS = 11, MeOH = 0, χ² = 14.42, d.f. = 1, p ≤ 0.001).

Figure 4. — (a) Near-source behaviour of pre-ovulated and ovulated female silver lamprey and ovulated sea lamprey in the quasi-natural stream experiments. Data are presented as the mean proportion of females that entered the 3 keto petromyzonol sulfate (3kPZS) baited nest (dark grey) or the methanol baited nest (light grey). (b) Upstream movement of pre-ovulated and ovulated female silver lamprey and ovulated sea lamprey in quasi-natural stream experiments. Data are presented as the mean proportion of females that moved upstream when 3kPZS (dark grey) or methanol (light grey) was applied. Error bars represent the standard error of the mean. Significant differences between the response to 3kPZS and response to methanol (α = 0.05) as determined using logistic regression are displayed with an asterisk. p-of sil, pre-ovulated female silver lamprey; of sil, ovulated female silver lamprey; of sl, ovulated female sea lamprey.

Table 1.

Near-source preference of pre-ovulated and ovulated female silver lamprey to 3 keto petromyzonol sulfate (3kPZS) as evaluated using a two-choice maze. The response of ovulated female sea lamprey to 3kPZS is shown for reference (N. Johnson 2009, unpublished data). Control = number of lampreys that preferred the control channel, 3kPZS = number of lampreys that preferred the 3kPZS channel. Index of preference = [ae/(ae + be) − ac/(ac + bc)], where bc is before odour in control channel, be is before odour in experimental side, ac is after odour in control channel and ae is after odour in experimental channel. p-values were determined using a Wilcoxon signed-rank test (α = 0.05).

subject	control	3kPZS	index of preference (s.e.)	p-value
pre-ovulated female silver lamprey	5	9	0.11 (0.09)	0.27
ovulated female silver lamprey	7	4	−0.06 (0.09)	0.28
ovulated female sea lamprey	1	10	0.3 (0.08)	0.01

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4. Discussion

Our data show that the female preference for a component of the male sea lamprey mating pheromone may be the result of a sensory trap. Spermiating male sea lamprey direct ovulated females to nests by releasing a bile alcohol signal, 3kPZS, at exaggerated rates [18,27,28,29]. We suggest that female preference for 3kPZS evolved through a non-sexual mechanism. Specifically, we hypothesize that silver lamprey, a basal member of the Petromyzontidae [30–35], cue onto larval-released 3kPZS to locate streams containing productive habitat conducive to offspring survival and that males have not adapted to take advantage of the preference by signalling with 3kPZS. In support of this hypothesis, we found that (i) 3kPZS was released by silver lamprey larvae at rates similar to putative sea lamprey migratory cues [36]; (ii) more migratory females moved upstream in response to 3kPZS, and spawning-phase silver lamprey females retained the upstream movement response to 3kPZS; and (iii) spawning-phase silver lamprey males did not release 3kPZS at the exaggerated rate observed in sea lamprey. Based upon the above findings, we infer that the female preference for 3kPZS evolved via natural selection in silver lamprey, and exaggerated signalling evolved later in the sea lamprey.

Alternative forms of male competition observed in sea lamprey and silver lamprey may have caused females to locate nests based on the odour of individual males (sea lamprey) or the odour of small spawning groups (silver lamprey). Most lampreys, including silver lamprey, spawn cooperatively, typically with two to three males per spawning nest [41–45]. The sea lamprey appears to be an exception, and typically displays intense male competition and aggression [41] (one male per spawning nest). The male competition in sea lamprey may have placed strong selective pressure on males to lure females with an exaggerated trait (3kPZS), whereas the communal spawning of silver lamprey may have pressured males to compete on a different level, perhaps through a form of sperm competition. Silver lamprey females may locate a nest using the collective odour of multiple males. However, our data did not support that female silver lamprey locate nesting males using the 3kPZS released by a group of two to three spawning males. Spermiating male silver lamprey released 3kPZS at approximately 200 ng h⁻¹, compared with the 49 000 ng h⁻¹ released by spermiating male sea lamprey. Based on a release rate of 200 ng h⁻¹, the 3kPZS released by one silver lamprey would activate a spawning nest to a concentration to approximately 1 × 10⁻¹⁵ M (nest width = 0.6 m, velocity 1.0 m s⁻¹ [41], nest cavity depth = 0.08 m [42]). Activation to a concentration of 1 × 10⁻¹² M, the detection threshold as determined using electrophysiological studies for sea lamprey [46], would require approximately 1000 male silver lampreys. A female in extremely close proximity may be able detect the 3kPZS released by a silver lamprey male; however, female silver lamprey did not show any near-source behavioural responses to 1 × 10⁻¹² M 3kPZS. The inability of ovulated female silver lamprey to locate the source of 3kPZS matches the hypothesis that the female preference evolved as a migratory behaviour and is not an adaptation in taking advantage of the minute amount of 3kPZS released by males. Larval habitat and spawning habitat do not overlap, as larvae require mucky sediment in which to burrow [47], and spawning adults require rocky substrate in which to construct nests [41]. Although entering the stream containing 3kPZS released by larvae is probably adaptive for females, locating the source of larval odour is unlikely to be adaptive for females given that males have not evolved to signal with 3kPZS.

Female preference arising from a sensory trap may need to be mutually adaptive to be maintained in a sexual context [48] and can be strengthened by sexual selection when mutually adaptive [49]. Although female preference for 3kPZS appears to have originated via natural selection, our data indicate that the behaviour has been strengthened in the sea lamprey. Ovulated female silver lamprey display general upstream movement behaviours in response to 3kPZS, useful for locating streams with successful larvae, but not mate location. In comparison, ovulated female sea lampreys are strongly attracted to the source of 3kPZS, a sexual behaviour useful in locating nesting males [28]. The strengthening of the response in sea lamprey may represent a switch from a deceptive to an honest signal [50]. Such a transition requires (i) uncoupling of the sexual response from the original non-sexual cue and (ii) female use of the male trait as an indicator of mate quality during mate selection [51]. Although the uncoupling of the behaviours is apparent in the honed response observed in sea lamprey, the relation of 3kPZS release to male fitness and its involvement in female mate choice is unknown.

Recent phylogenetic studies indicate that male signalling and female preference can be lost or weakened through relaxed sexual selection or increased pressures of natural selection [52]. Thus, while we interpret the lack of male signalling and weak female preference in silver lamprey as evidence that male signalling and strong female preference in sea lamprey represents the derived character state, the alternative possibility that female preference and male signalling in silver lamprey has weakened remains. Differences in fitness costs/benefits, possibly a result of polygynandry, may have driven a weakening in male signalling and female preference in silver lamprey. Two lines of evidence support the role of a receiver bias instead of the alternative hypothesis that 3kPZS signalling in silver lamprey has weakened. First, the broad occurrence of polygynandry across lampreys indicates that polygyny in sea lamprey represents a derived state and that polygynandry is the ancestral state [41–45]. Male competition via pheromone signalling is unlikely in communal spawning lampreys, as the odour of males probably mixes thoroughly on a nest. Therefore, the mating system, and likewise the signalling system, observed in sea lamprey probably represents the derived character state. Second, our results showing a non-sexual source of 3kPZS and behavioural responses fitting in a non-sexual context provide support for the role of natural selection, rather than sexual selection, driving female preference for 3kPZS in silver lamprey.

The chemical communication system employed by lamprey offers a useful example of the mechanism through which a signal may have evolved. Bile salts function as endocrine signalling molecules, regulating numerous physiological pathways by binding to, among others, G-protein-coupled receptors (GPCRs [53]). Odourants are thought to bind to receptors belonging to the GPCR superfamily [54]. A mutation externalizing GPCRs to the olfactory epithelium would allow individuals to detect conspecific bile fluids [14,55]. The cognitive and behavioural responses to 3kPZS probably evolved and were strengthened by the reliability of larval odour as an indicator of offspring success, a cue that becomes critical during the extensive migration of lampreys to rearing grounds [39]. Male silver lampreys appear to possess the physiological capacity to release 3kPZS, but do so at an unexaggerated rate. The emergence of polygyny in sea lamprey probably placed strong selection on individual male sea lamprey to exaggerate the release of 3kPZS [18]. Sea lamprey males releasing large amounts of 3kPZS gain the fitness benefit of luring females to the spawning nest.

In summary, we present data indicating that in the sea lamprey sexual communication system, the female preference for the male-released bile alcohol, 3kPZS, may have originated as a result of a sensory trap. We infer that in the ancestral silver lamprey larval-released 3kPZS functions as a migratory cue that guides females into habitable streams and male silver lamprey have not evolved to manipulate the female preference by releasing 3kPZS at the high rates observed in the sea lamprey [18]. Finally, we suggest that the chemical communication system of lampreys offers not only a useful model to study aquatic pheromones [23], but may also prove useful in providing empirical evidence for communication theory, which often focuses on the auditory and visual senses [56].

Acknowledgements

The staff of the US Geological Survey Hammond Bay Biological Station provided research facilities and guidance. The US Fish and Wildlife Service Marquette and Ludington Biological Stations assisted in collecting lampreys. Dr Janette Boughman, Cory Brant and three anonymous reviewers provided comments that greatly improved the manuscript. Thanks to Ed Benzer, Ethan Buchinger, Christopher Dean, Phil Ganz, Hugh McMath and Jeff Yaklin for field assistance.

Funding statement

Funding was provided by the Great Lakes Fisheries Commission. Mention and use of trademark products does not constitute endorsement from the US Government. This article is contribution 1784 of the US Geological Survey Great Lakes Science Center.

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PERMALINK

Evidence for a receiver bias underlying female preference for a male mating pheromone in sea lamprey

T J Buchinger

H Wang

W Li

N S Johnson

Abstract

1. Introduction