Abstract

The birds-of-paradise (Paradisaeidae) exhibit some of the most diverse color patterns and courtship displays among species. Paradoxically, birds-of-paradise hybridize more frequently than other birds, even hybridizing across species and genera with remarkably divergent color patterns. Hybridization among such distinctly colored species might suggest that reinforcement was unimportant for color pattern divergence because reinforcement favors trait divergence that reduces the likelihood of hybridization over time, and is expected to eliminate hybridization between species. Here I present an alternative view: that persistent but infrequent hybridization among species that differ markedly in prezygotic isolating traits, such as color pattern in birds, represents the signature of historical reinforcement, and occurs when (i) divergence in single traits can reduce, but not prevent, hybridization, (ii) trade-offs constrain the divergence of prezygotic isolating traits, and (iii) selection against hybrids is weak when hybrids are rare. Considering these factors, the paradox of the birds-of-paradise—where species with distinct prezygotic isolating traits are more likely to hybridize at low frequencies—is the expected outcome of reinforcement. Sexual selection by female choice could further intensify the effects of reinforcement, particularly if reinforcement directs sexual selection to different traits in hybridizing populations. This latter process could potentially explain the exceptional diversity of extravagant ornaments in the birds-of-paradise.

Highlights

  • If reinforcement was important in the evolution of color patterns, we might expect distinctly colored species of birds to hybridize less frequently than colored species because reinforcement favors trait divergence that reduces the likelihood of hybridization over time, and is expected to eliminate hybridization between species (Coyne and Orr 2004: 66)

  • Reinforcement could be important in birds, but instead act on female discrimination rather than male color pattern (Price 2008), leaving male color pattern divergence uncorrelated with the likelihood of hybridization among species

  • I follow with evidence to support the mechanisms underlying the predicted patterns in the case of hybridization, reinforcement, and the divergence of color pattern and other prezygotic isolating traits

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Summary

Reinforcement and the divergent evolution of species

Reinforcement is thought to favor individuals with color patterns that are more divergent from closely related species because these individuals are less likely to mate with the wrong species, which is costly (Figure 1c, Servedio and Noor 2003). Within the broad time frame after reinforcement has occurred, but before complete isolation has evolved, a greater incidence of hybridization among phenotypically distinct species (Figure 1d) should be a common pattern among organisms that have diverged by reinforcement, not just birds We should expect this relationship for the same reasons: (i) the likelihood of hybridizing is unlikely to be controlled by one trait, (ii) prezygotic traits should frequently encounter trade-offs and constraints, and (iii) reinforcement should reduce, but not eliminate, hybridization because selection against hybrids is weak when hybrids are rare. If females prefer the most extravagant expression of a trait, and diverging populations differ in their extravagance, females of two populations may favor the more extravagant males of one population, increasing rates of hybridization (Randler 2002, Figure 2) In both of these examples, if hybrids are unfit, the increased hybridization could increase the potential for reinforcement, provided gene flow is not excessive (Servedio and Noor 2003). Such a process could potentially explain another mystery of the birds-of-paradise: why species show such diverse sexual ornamentation across species, with different traits elaborated in different species (including extravagant breast, tail, crown, scapular, and other feathers, legs, bills, eyes, skin patches, mechanical sounds, vocalizations, courtship displays, and other behaviors; Frith and Beehler 1998, Laman and Scholes 2012)

Persistent hybridization as a signature of historical reinforcement
Response to referee

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