Evolution was once thought to work exclusively as a gradual process (Darwin, 1859), where speciation followed the accumulation of divergent traits primarily in isolated populations (Carroll et al., 2007). Yet decades of research have transformed this model of evolution into one that emphasizes the importance of behavior (Lapiedra et al., 2018; Grant and Grant, 2010), while accommodating not only rapid phylogenetic and phenotypic diversification (Rudh et al., 2011; Uy and Borgia, 2000; Kettlewell, 1956), but also speciation with gene flow (Servedio, 2016; Servedio, 2004; Kopp et al., 2018). Theory predicts that such instances of rapid speciation may occur provided there is sufficient phenotypic disparity between diverging population to erect reproductive barriers, but this implies that other factors that give rise to phenotypic variation also play an important role in this process. One of these factors is an organism’s physiology, which provides the functional architecture that defines how phenotypes can evolve and/or emerge anew. However, studies rarely explore the role of certain physiological systems in the process of sympatric speciation, creating a gap in our understanding of modern evolutionary biology.

A major way that physiology influences evolution is through constraint, due to numerous trade-offs between systems or processes that function in a mutually exclusive manner (Roff and Fairbairn, 2007; Alexander, 1985). Skeletal muscle performance is a prime example of this phenomenon: its design entails performance traits that are inversely related to each other, such as between speed and endurance (Vanhooydonck et al., 2014; Wilson et al., 2002). At the same time, skeletal muscle also actuates many sexually-selected behaviors that act as the basis for mate choice (Goller and Suthers, 1996; Garcia et al., 2012; Fuxjager et al., 2017a). This suggests that performance trade-offs inherent to muscle itself can impede the formation of reproductive barriers, particularly in cases where behavioral divergence should mediate speciation. Evaluating this idea requires a simultaneous examination of a species’ evolutionary history, as well as whole-organism and muscle performance. Few studies unite all three perspectives, however, leaving an unclear relationship between animal design, behavior, and evolutionary process.

Here, we address this issue by exploring how performance trade-offs borne out via skeletal muscle shaped the evolution of sexual display behavior during a rapid speciation event. We study a small genus of Neotropical birds called bearded manakins (Aves: Pipridae). This group last shared a common ancestor roughly 300,000 years ago (Brumfield et al., 2008; Tello et al., 2009), before splitting into four species: white-bearded manakins (M. manacus), golden-collared manakins (Manacus vitellinus), white-collared manakins (M. candei), and orange-collared manakins (M. aurantiacus). We specifically examine how disruptive selection operates on one of the bird’s main courtship signals—the roll-snap—to generate phenotypic divergence sufficient to facilitate assortative mating (Servedio, 2016). Males produce this behavior by rapidly hitting their wings together over their back, generating a mechanical trill-like sound (Fuxjager et al., 2017a). The result is a repetitive rhythmic signal, which is a common signal type in animal courtship (Mowles and Ord, 2012). These displays convey information through multiple component signals, but one of particular importance in reshaping a receiver’s behavior is signal speed (Schuppe and Fuxjager, 2018; Ord et al., 2007; Podos, 2001). As such, we hypothesize that speed is an important feature of roll-snap performance. Although the degree to which roll-snap speed itself is sexually selected remains unknown, previous studies in golden-collared manakins show that females discriminate millisecond-scale differences in other displays and prefer to mate with males that display faster (Barske et al., 2011). Therefore, the speed with which a male hits his wings together likely functions as an important courtship signal that is subject to strong sexual selection. If so, then small changes in female preferences for speed may provide the selection pressure necessary for display divergence. However, disruptive selection may not be able to freely drive sister species to exhibit opposite patterns of directional selection for this trait, largely because the speed with which skeletal muscles control wing movements is constrained by important performance trade-offs, such as one between speed and endurance (Vanhooydonck et al., 2014; Wilson et al., 2002). This leads to the question: what role did intrinsic muscle performance trade-offs play in the rapid diversification of these species?

As a first step toward answering the question posed above, we evaluated whether speciation of bearded manakins occurred under sympatry, a special case of speciation with gene flow (Kopp et al., 2018). We accomplished this using phylogeographic models (O'Donovan et al., 2018; Lemmon and Lemmon, 2008; Pagel et al., 2004) to reconstruct the ranges of ancestral Manacus populations (Figure 1a). The model output (Figure 1b) shows that the bearded manakins’ most recent common ancestor occupied a geographic range similar to that of the western population of extant white-bearded manakins, giving rise to this species before migrating west across the Isthmus of Panama (Video 1). Golden-collared manakins were the next to split off, emerging in a geographic range that overlapped between 49% and 73% (95% credible intervals) with that of the final common ancestor to both white-collared and orange-collared manakins. This wide-ranging ancestral overlap is therefore consistent with speciation occurring in sympatry, typically considered to occur when ranges overlap ≥25% (Seddon, 2005; Cooney et al., 2017; Tobias et al., 2014). Furthermore, because modern bearded manakins are mostly allopatric (Figure 1c), geographic isolation of these birds likely followed their diversification, rather than preceding it. This is consistent with previous work in golden-collared and white-collared manakins, which hybridize readily in a small region of range overlap in Panama (Parsons et al., 1993). In the hybrid zone, directional selection for plumage ornaments is strong enough for golden-collared manakin traits to cross the hybrid zone and introgress into the white-collared manakin population (Parsons et al., 1993; McDonald et al., 2001; Brumfield et al., 2001). Moreover, whole-genome analysis of the two species finds high rates of introgression and genetic differentiation at a wide range of unrelated loci, which is consistent with an evolutionary history characterized by reproductive isolation following adaptive divergence in various traits (Parchman et al., 2013). Thus, mechanisms other than those linked to geographic isolation likely help drive rapid speciation in the genus.

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Video 1

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If courtship display divergence played a role in speciation, then species arising with gene flow should exhibit different display phenotypes. We therefore examined species differences in the acrobatic roll-snap display by analyzing acoustic recordings of roll-snaps for each species (Table 1), measuring both signal speed (snaps s⁻¹) and length (total number of snaps). Speed differed significantly among the species (Figure 2a; F_3,146=9.203, p<0.0001), with golden-collared manakins producing the fastest roll-snaps, white-bearded and white-collared manakins (no ancestral overlap) both producing intermediate speed roll-snaps, and orange-collared manakins producing the slowest roll-snaps. The magnitude of mean differences is relatively small overall (<5 Hz), but also reflects larger differences in the upper range of display speed. For example, the fastest roll-snap observed in white-collared manakins (61 Hz) falls within the interquartile range of the golden-collared manakin’s speed distribution [55.9,61.1]. Because phenotypic constraints typically impact trait evolution by restricting the extremes of a distribution (Wilkins et al., 2013), this suggests that shifting constraint space may underlie differences in speed. At the same time, we found that roll snap length in all four species was statistically indistinguishable (Figure 2b; F_3,153=0.229, p=0.876). Therefore, the roll-snap diverged among species exclusively in terms of signal speed (i.e. snap repetition rate), but not in terms of the total number of snaps. Therefore, if females attend to differences in roll-snap speed as they do with other signals (Barske et al., 2011), conspecific mate preference should be reinforced by divergent roll-snap speeds (McDonald, 1989). Our data are thus consistent with a model in which phenotypic divergence among sympatric populations plays a role in supporting assortative mating (Servedio, 2016; Kopp et al., 2018).

Figure 2

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Figure 2—source data 1

Data_acoustics.txt: Measurements of roll-snap speed and length obtained from audio recordings of displaying birds.

Includes accession numbers for locating the original recordings on internet archives.

https://doi.org/10.7554/eLife.40630.006

Download elife-40630-fig2-data1-v1.txt

Evolutionarily modifying a signal to become faster can sometimes incur costs to other performance attributes, such as endurance (Van Damme et al., 2002; Vanhooydonck et al., 2001; Reidy et al., 2000, c.f. Sorci et al., 1995). Divergence in the roll-snap may therefore be constrained by these trade-offs, especially in species that evolve faster—but equally as long—roll-snaps. To examine whether this evolutionary impasse is present, we used quantile regression to test for an inverse relationship between the speed and length of each species roll-snap (Cade and Noon, 2003; Koenker and Machado, 1999; Miles et al., 2018; Wilson et al., 2014). The mere existence of such a relationship would indicate that a given species was signaling near (or at) its phenotypic limit with respect to these measures of performance. Indeed, at the uppermost testable quantile (τ = 0.9), we detected this trade-off in both golden-collared (Figure 3a; t = -4.03, p<0.001) and white-collared manakins (Figure 3b; t = -2.76, p=0.007), but not in white-bearded (Figure 3c; t = -0.36, p=0.722) and orange-collared manakins (Figure 3d; t = -0.70 p=0.490). Roll-snaps are therefore differentially constrained across species.

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Even among two species undergoing a performance constraint between speed and endurance, there can be variation in terms of the trade-off’s steepness (slope), as well as the proportion of individuals in the population that encounter it. If the trade-offs we uncover are the result of endurance costs, then the negative linear relationship between speed and length should be steeper in the species with the faster display (i.e. golden-collared manakins, see Figure 2a). This was indeed the case (F_1,230=22.1, p=0.001), supporting the notion that performance costs to speed become greater as selection drives the evolution of the signal further into the constrained trait-space. Similarly, because golden-collared manakins have a faster display overall than white-collared manakins (post-hoc: z = 2.5, p=0.038), more individuals should produce displays fast enough to encounter endurance constraints. Our data again support this idea, as nearly all golden-collared manakins (top 80% of the population) experience a cost to display speed (Table 2), given the signal’s length (Figure 3a; at τ = 0.2: t = -2.95, p=0.004), whereas only the top 20% of white-collared manakins display fast enough to experience such a cost (Figure 3b; at τ = 0.8: t = -2.33, p=0.028). Thus, for these two species, the rate at which an individual snaps its wings together to display is influenced by the inverse relationship between speed and endurance, with the effect of this constraint appearing greater in golden-collared manakins. This may be a consequence of the fact that golden-collared manakins have a faster roll-snap than the other species, but without a change in overall display length. Their roll-snap speed appears to have diverged just enough to maintain the signal’s length, with trade-offs consequentially appearing at the level of the individual.

The origin of behavioral trade-offs may lie in the physiological and/or morphological underpinnings of display production (Podos, 2001; Derryberry et al., 2012). For the roll-snap, skeletal muscle performance may be one of the limiting factors, considering that muscle tissue itself is thought to be the origin of the speed-endurance trade-off (Vanhooydonck et al., 2014; Wilson et al., 2002; Bottinelli et al., 1994). In bearded manakins, the scapulohumeralis caudalis muscle (SH, Figure 4a) is the primary actuator of the roll-snap—it contracts when a male’s wings are raised vertically above its back, causing the wrists to collide (snap) over the axial mid-line (Fuxjager et al., 2017a). Otherwise, the SH is a flight muscle, acting as a ‘strut’ during powered locomotion by rotating and retracting the wing (Dial, 1992). Past work shows that bearded manakins maintain an extremely fast SH, likely due to selection for a fast display (Barske et al., 2011; Fuxjager et al., 2016a; Fuxjager et al., 2017b); thus, one might expect that the evolution of SH speed contends with a decrease in endurance. To test this idea, we quantified muscle performance first in the golden-collared manakin (the fastest species) and then in the white-collared manakin. Although the white-collared manakin was not the species with the slowest roll-snap, we chose it as a basis of comparison due to the well-studied evolutionary history between these two populations. White-collared and golden-collared manakins are the only pair of Manacus species that are well known to hybridize today (McDonald et al., 2001), which means that signal divergence is likely important to mediating reproductive barriers in the present day.

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Data_fatigue.txt: Contractile phase measurements collected from each twitch cycle during stimulation of golden-collared and white-collared manakin SH muscles.

https://doi.org/10.7554/eLife.40630.012

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We used in situ recordings of SH twitch speed (Fuxjager et al., 2016a; Fuxjager et al., 2017b) to test whether skeletal muscle performance underlies differences in display behavior. Accordingly, we measured the percent relaxation of the SH at different stimulation frequencies (30–100 Hz), modeling relative relaxation (0–100%) as a function of muscle stimulation speed (Figure 4b). Our results confirmed previous work (Fuxjager et al., 2016a) by indicating that golden-collared manakins maintain an extremely fast SH—that is, this muscle relaxes more quickly at high frequencies than it does in white-collared manakins (Figure 4c; model difference: F_3,49=15.2, p<0.001). The muscle therefore also maintains a significantly greater half-relaxation frequency in the golden-collared manakin, which is the maximum frequency at which the muscle contracts and relaxes at 50% of its predicted functional range (Figure 4d; F_1,49=79.8, p<0.001). Next, to determine if the ability of the SH to perform at such speeds is limited by endurance costs, we modeled the tissue’s percent relaxation as a function of the stimulation pulse number (1-8) at each given stimulation frequency. This reflects how the muscle’s performance changes at different speeds in response to repeated stimulations. We found that the golden-collared manakin SH relaxed between 75% and 100% when stimulated at 50, 60 and 70 Hz (Figure 5a). However, when stimulated at ≥80 Hz, its percent relaxation significantly declined with each twitch (Figure 5a and Table 3; F_1,12=18.7, p=0.005 at 80 Hz; F_1,12=33.9, p<0.001 at 90 Hz; F_1,12=22.8, p=0.003 at 100 Hz). Indeed, we find that the level of relaxation dropped from around 75–100% during the first contraction to around 20–50% as the stimulation train progressed. By contrast, in the white-collared manakin, percent relaxation of the SH never changed across any of the stimulation trains (Figure 5b and Table 3). Instead, only overall percent relaxation decreased with increasing frequency (see above, Figure 4c). These data therefore suggest that the golden-collared manakin SH experiences a form of ‘rapid fatigue’ when stimulated at especially fast frequencies. This performance attribute contrasts with fatigue as it is normally discussed, where the latter is typically defined as a decrease in speed and force production over periods of time greater than the fractions-of-a-second that we show herein (Wilson et al., 2002; Allen et al., 2008). Nonetheless, we expect that the ability to resist this ‘rapid fatigue’ similarly qualifies as a form of muscle endurance per se (the ability to resist fatigue; Wilson et al., 2002).

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To further examine how this divergence in SH performance relates to display behavior, we modeled the way that the observed ‘rapid fatigue’ changed in response to stimulation frequency. As such, we first computed the slopes that describe the relationships between percent relaxation and stimulus number within the different stimulation trains (see above; Figure 5a and b). We then plotted these values as a function of overall stimulation frequency, finding that the SH of the golden-collared manakin experiences a progressively greater decline in performance when stimulated at high speeds (Figure 5c; F_1,6=27.7, R² = 0.82, p=0.002). This effect is absent in white-collared manakins (Figure 5c; F_1,7=0.15, R² = 0.02, p=0.710), which instead maintain a constant (fused) state when subjected to the same fast stimulation frequencies. Importantly, for the golden-collared manakin, we show that the upper confidence limit of this regression line crosses 0 at ≈60 Hz—a value that represents the relative speed at which the trade-off with endurance should begin to manifest. This roughly correspond to the species’ average roll-snap speed, which is 58.4 Hz (Figures 2a and 5c). Thus, sexual selection in golden-collared manakins has likely driven the evolution of the roll-snap to its maximal speed, such that it is produced at the SH’s performance limit due to the tissue’s intrinsic trade-off with endurance. Further support for this idea comes from a subsequent analysis, in which we found that male golden-collared manakin produce significantly shorter roll-snaps when they are at or above 60 Hz, compared to less than 60 Hz (β = −4.32, F_1,119=46.7, p<0.001; Figure 5—figure supplement 1).

What explains the rapid decline in relaxation with multiple contractions at high speed? Distinct mechanisms may shape the different phases of the contraction-relaxation cycle; thus, we quantified shortening and lengthening periods in twitch recordings that were both (i) right above each species’ average roll-snap speeds (golden-collared manakin threshold = 60 Hz, white-collared manakin threshold = 58 Hz) and (ii) at a high frequency stimulation (80 Hz) (Figure 6). Both measures showed considerable variation, but for both species we found no significant changes within the twitch series (p_min = 0.20; Figure 6). This indicates that shortening and lengthening duration remained consistent during the stimulation trains. Nonetheless, in the golden-collared manakin, we know that percent relaxation declines at high stimulation frequencies in this same timeframe. Thus, the overall ‘rapid fatigue’ response is likely a result of decreased capacity for relaxation, pointing to processes underlying this event as a potential limiter of muscle performance. This may be linked to constraints on calcium buffering and/or re-uptake mechanisms, given they play an important role in setting muscle relaxation rates (Syme and Josephson, 2002; Rome et al., 1996). Regardless of which cellular mechanism ultimately limits SH performance in the golden-collared manakin, this is consistent with the fundamental framework of selection contending with constraint—the phenotype favored by selection (in this case, display speed) will evolve following directional selection until it is impeded by the underlying rate-limiting mechanism. In this case, it appears that the golden-collared manakin SH has been modified to allow the muscle to sustain rapid contraction-relaxation cycling, but different components of myocytic machinery have likely evolved in a mismatched fashion.

Figure 6

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Figure 6—source data 1

Data_twitchspeed.txt: Twitch speed measurements collected from muscle recordings of golden-collared and white-collared manakin SH muscles.

https://doi.org/10.7554/eLife.40630.016

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At the cellular level, muscle relaxation requires both rapid cross-bridge detachment and swift calcium cycling (Syme and Josephson, 2002; Rome et al., 1996). Past work in the golden-collared manakins suggests that the SH can achieve the former, with measures of maximal shortening velocity surpassing the maximum roll-snap speed (Fuxjager et al., 2016a). Thus, the factor that limits SH speed for more than two or three twitches—if not related to cross-bridge detachment rates—is likely related to processes governing calcium cycling within the myocyte (Syme and Josephson, 2002). This is indicative of evolutionary discordance between different facets of the muscle’s contractile machinery, which ultimately put the brakes on sexual selection for a rapid display. Further evolutionary elaboration of the roll-snap speed would likely require modifications to the calcium handling properties, alongside other adaptations for the performance of this signal in bearded manakins (Friscia et al., 2016; Fuxjager et al., 2016b; Fuxjager et al., 2016c). Notably, limitations to muscular calcium handling are not typically associated with the speed-endurance trade-off, which is often considered to result from muscle fiber type composition (Rivero et al., 1993; Komi, 1984; Esbjörnsson et al., 1993). This discrepancy is likely the result of differences between the so-called ‘rapid fatigue’ we observe and the more standard muscle fatigue that occurs when performance is depleted after prolonged muscle use.

General discussion

This study provides a blueprint that outlines how trade-offs in skeletal muscle performance influence a rapid sympatric speciation event. We use bearded manakins, which are Neotropical birds that separated into distinct species relatively recently. Our results show that the species in this complex evolved in a geographic scenario characterized by considerable range overlap, which means that that rapid speciation was likely facilitated by strong assortative mating (Servedio, 2016; Kopp et al., 2018). Bearded manakin divergence took place after ancestral populations migrated northwest out of Amazonia, across the Andes, and along the Isthmus of Panama. When the golden-collared manakin first diverged from its shared common ancestor with white- and orange-collared manakins, its range spanned the entire isthmus. As the species split, their roll-snap speeds also diverged for the three taxa that were ancestrally sympatric, and their ranges also began contracting to generate the (mostly) allopatric configuration seen today (Video 2). Specifically, we found that the golden-collared manakin’s roll-snap increased in speed, presumably at the same time as its SH was modified to support the especially rapid contraction-relaxation cycling that was necessarily to generate the movements that make up this behavior. The underlying driver for signal and range differentiation may have been shifts in female preferences for male courtship display performance (Kopp et al., 2018; Servedio and Burger, 2014). Alternatively, emergent differences in roll-snap speed may have supported conspecific mate preference independently of directional selection for speed. This may explain why orange-collared manakins, which are not known to hybridize with golden-collared manakins, uniquely exhibit a sharp decrease in roll-snap speed as their range moved south of the sympatric ancestral range. By contrast, the white-collared manakin (which did not undergo a large degree of speed differentiation) still interbreeds with golden-collared manakins where their ranges overlap. It also remains possible that other aspects of the roll-snap phenotype not assessed here—for example, the display’s amplitude or modulation thereof—may play a similar role in supporting divergence, but this remains to be seen.

Video 2

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During the parallel differentiation of species, plus their ranges and display phenotypes, the golden-collared manakin alone exhibited an increase in roll-snap speed. Such a change should incur some cost to the signal’s length, but we found no matching macroevolutionary shift in roll-snap length. Instead, a trade-off between speed and endurance is apparently borne out at the population level (rather than a macroevolutionary one), where only the species that evolved faster displays experience a trade-off between speed and length. We then show that this evolutionary pattern is explained by contraction-relaxation cycling kinetics in the skeletal muscle that actuates the roll-snap display—namely the SH. Thus, the species with the fastest display, the golden-collared manakin, also has the fastest SH. Further analysis of SH performance, however, reveals that this same bird also undergoes a decline in percent relaxation over repeated contractions at speeds greater than 60 Hz, which corresponds to the species’ average roll-snap speed. This helps explain why the SH appears to be faster than the bird’s actual display—that is, an intrinsic trade-off between muscle speed and endurance (length) blunts any potential effect of sexual selection for a faster display. Finally, we separately examined whether this endurance ‘cost’ to speed influences the duration of contraction and relaxation within a stimulation series, and we find that the timing of these two variables remain constant across multiple stimulations. Importantly, these effects occur despite the muscle showing an overall decline in percent relaxation, which points to the process of relaxation in and of itself as the origin of phenotypic constraint on roll-snap evolution.

Altogether, our data show how muscle physiology can influence the process by which divergent selection drives phenotypic evolution to support speciation with gene flow. Indeed, for the nascent radiation of tropical bearded manakins, this processes likely partially hinges on changes to an acrobatic mating dance that inextricably linked to the muscular control of behavioral outflow. Thus, if selection on this display is to proceed, it must contend with constraints imposed by this tissue’s design. We provide a glimpse into how this might occur, while also showing that additional changes are necessary to the muscle for selection on the golden-collared roll-snap to proceed further. Of course, other traits like plumage ornamentation have also diverged due to sexual selection (McDonald et al., 2001), although recent work suggest sexual dichromatism alone is not likely to facilitate species coexistence or speciation in sympatry (Cooney et al., 2017). Nonetheless, our study supports the idea that organism’s physiological design is critical for creating the landscape in which phenotypic evolution occurs, and therefore contributes to the process by which species diverge.

All data generated or analyzed during this study are included in the manuscript and supporting files.

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Author details

1. Meredith C Miles

   Wake Forest University, Winston-Salem, United States

   Contribution

   Formal analysis, Investigation, Methodology, Writing—original draft, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7307-0195

2. Franz Goller

   1. University of Utah, Salt Lake City, United States
   2. Institute for Zoophysiology, University of Münster, Germany

   Contribution

   Formal analysis, Investigation, Methodology, Writing—review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-5333-1987

3. Matthew J Fuxjager

   Wake Forest University, Winston-Salem, United States

   Contribution

   Conceptualization, Resources, Formal analysis, Supervision, Funding acquisition, Investigation, Methodology, Writing—original draft, Project administration, Writing—review and editing

   For correspondence

   mfoxhunter@gmail.com

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0591-6854

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