Role of sexual imprinting in assortative mating and premating isolation in Darwin’s finches Peter R. Granta,1 and B. Rosemary Granta aDepartment of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ 08544 Contributed by Peter R. Grant, September 11, 2018 (sent for review August 8, 2018; reviewed by Darren Irwin and Carel ten Cate) Global biodiversity is being degraded at an unprecedented rate, as shown by the numerous examples of introgressive hybridiza- so it is important to preserve the potential for future specia- tion between recently formed species (reviewed in refs. 10–13). tion. Providing for the future requires understanding speciation Important questions that need to be addressed are how the as a contemporary ecological process. Phylogenetically young barrier is constructed, how it evolved, why it occasionally leaks, adaptive radiations are a good choice for detailed study because and how gene exchange affects the evolution of the respective diversification is ongoing. A key question is how incipient species populations (14). Paradoxically, the breakdown of reproductive become reproductively isolated from each other. Barriers to gene isolation may be especially informative in answering questions exchange have been investigated experimentally in the laboratory about how it was established by exposing candidate traits that and in the field, but little information exists from the quantitative constitute the normally effective barrier to interbreeding (15– study of mating patterns in nature. Although the degree to which 17). Further insights can then be gained by conducting experi- genetic variation underlying mate-preference learning is un- ments on the genetic and experiential basis of mate choice and known, we provide evidence that two species of Darwin’s finches preferences of closely related species (16, 18–22). imprint on morphological cues of their parents and mate assorta- Here we describe the results of a long-term field investigation tively. Statistical evidence of presumed imprinting is stronger for into mating patterns of Darwin’s finches in the Galápagos ar- sons than for daughters and is stronger for imprinting on fathers chipelago, discuss their significance in the context of speciation, than on mothers. In combination, morphology and species-specific and comment on their relevance to the maintenance of bio- song learned from the father constitute a barrier to interbreeding. diversity. The finches are a young adaptive radiation comprising The barrier becomes stronger the more the species diverge mor- 18 ecologically diverse species (23). According to mitochondrial phologically and ecologically. It occasionally breaks down, and dating, they diverged from a common ancestor 2.3 (24) or 2.5 the species hybridize. Hybridization is most likely to happen (25) Mya and diversified in approximately the last 1 My (23). when species are similar to each other in adaptive morphological Previous work has illuminated the basis of reproductive isolation traits, e.g., body size and beak size and shape. Hybridization can of closely related species of the group (26–30), but unanswered lead to the formation of a new species reproductively isolated are questions of how mates are chosen from members of the from the parental species as a result of sexual imprinting. Con- same population and whether the rules of intraspecific mate servation of sufficiently diverse natural habitat is needed to sus- choice apply to the avoidance of heterospecific mating (31). This tain a large sample of extant biota and preserve the potential for is the subject of the present report. future speciation. The framework for our investigation is the hypothesis of sexual imprinting (reviewed in refs. 32 and 33). According to this hy- imprinting | assortative mating | hybridization | speciation pothesis, offspring learn morphological features of their parents in early life—they imprint on them—and the mental images are he enormously rich biodiversity of the planet poses two used by the fully grown offspring as cues when choosing a mate Tquestions to biologists: How to explain it and how to main- tain it. Understanding the origin of biodiversity involves the Significance evolutionary search for mechanisms of speciation. The mainte- nance of biodiversity in a world that is experiencing environ- It is important to preserve the potential for future speciation mental degradation on a global scale (1) appears to be an because global biodiversity is being rapidly degraded. A key entirely separate endeavor. In the short term, this is largely true, question is how incipient species become reproductively iso- except that the future for some species may hinge upon their lated from each other. Here we provide evidence that two evolutionary ability to respond to environmental stress, stress species of Darwin’s finches choose mates on the basis of that is both continuous and increasing as well as episodic and learning morphological features of their parents and possibly recurring (2). Termed “evolutionary rescue from the threat of from inherited preferences. The evidence for imprinting is extinction” (3), the responsiveness of species depends largely stronger in sons than in daughters and for imprinting by both upon the amount of standing genetic variation together with sons and daughters is stronger on fathers, which sing, than on mutation (4–7). In the medium to long term, we should be mothers, which do not. Imprinting establishes a barrier to in- thinking about how to maintain communities of organisms in a fit terbreeding between morphologically different species. The bar- state for future speciation: not just the prevention of extinction rier is leaky, species occasionally hybridize, and the hybrids can but the generation of new species. Unless environmental pro- give rise to a new species based on learned mate preferences. vision is made to allow for future speciation, the current re- duction in the number of species will be permanent. Therefore, Author contributions: P.R.G. and B.R.G. designed research, performed research, analyzed whatever can be learned about how species arise is useful in- data, and wrote the paper. formation for addressing the neglected problem of preserving Reviewers: D.I., University of British Columbia; and C.t.C., Leiden University. the potential for future speciation. The authors declare no conflict of interest. Speciation involves the formation of a barrier to the exchange Published under the PNAS license. of genes between two divergent lineages derived from one (8). 1To whom correspondence should be addressed. Email: [email protected]. The barrier may be intrinsic or extrinsic and may function pre- This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. EVOLUTION zygotically or postzygotically (9). In the early stages of divergence 1073/pnas.1813662115/-/DCSupplemental. the barrier is likely to be solely prezygotic and may be permeable, Published online October 22, 2018. www.pnas.org/cgi/doi/10.1073/pnas.1813662115 PNAS | vol. 115 | no. 46 | E10879–E10887 Downloaded by guest on September 25, 2021 (34, 35). An alternative view to learning-based mate preferences Results is that preferences are genetically inherited. Distinguishing be- The Influence of Imprinting on Mothers and Fathers in Mate Choice. tween learned and inherited predispositions will require experi- The first prediction of the imprinting hypothesis—that a chosen mental studies in the future (Discussion). We have chosen mate resembles the chooser’s parents—is supported in the two imprinting as a framework because of the abundant literature on species but in different ways (Table 1). For G. fortis mates, the early learning and mate choice consequences (32–36) in contrast body size of the female is strongly predicted by the body size of to a lack of evidence for genetic variation in mate preferences for the male’s parents, and the body size of the male mate is pre- metric traits in passerine birds with biparental care. dicted by the size of the female’s parents. In both cases the fa- The imprinting hypothesis predicts a similarity in the mor- ther’s size (Fig. 1) is a statistically stronger predictor than the phology of a chooser’s mate and the chooser’s parents. To the mother’s size. extent that morphological cues are heritable (37), a second In contrast to the G. fortis results, the G. scandens male’s choice prediction is that mates should resemble each other (assortative of a mate is not predicted by the size of either of his parents. mating). This follows from the fact that the imprinted mor- However, the beak shape of a female’s parents is a statisti- phology of mother and father is both a genetic predictor of the cally strong predictor of her mate’s beak shape. The pre- offspring and a cultural predictor of the offspring’s mate. These diction is significant for the father’s but not for the mother’s predictions apply to members of the same species. However, beak shape. A separate analysis of beak variables shows that closely related species may be similar morphologically and the beak shape association stems from beak length and not therefore, as in other organisms, prone to hybridize (13, 38, 39). beak depth or beak width, whereas for G. fortis beak depth is A third prediction of the imprinting hypothesis is that the indi- the primary predictor. viduals that hybridize should be more similar to the other species Nonrandom Mating. The second prediction of assortative mating than are nonhybridizing individuals, and a fourth prediction is on the basis of body size is supported by statistically strong that their parents should also be more similar to the other spe- positive correlations between mates in both G. fortis and G. cies than are nonhybridizing individuals. scandens (Fig. 2 and Table 2). Further, there is strong support for We have taken advantage of small island populations whose assortative mating by beak size [principal component (PC) pedigrees can be documented to answer questions of mate scores] in G.