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Experimental Evidence for Ovarian Hypofunction in Sparrow Hybrids Fabrice Eroukhmanoff1*, Melissah Rowe1,2, Emily R

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Experimental Evidence for Ovarian Hypofunction in Sparrow Hybrids Fabrice Eroukhmanoff1*, Melissah Rowe1,2, Emily R Eroukhmanoff et al. Avian Res (2016) 7:3 DOI 10.1186/s40657-016-0038-1 Avian Research RESEARCH Open Access Experimental evidence for ovarian hypofunction in sparrow hybrids Fabrice Eroukhmanoff1*, Melissah Rowe1,2, Emily R. A. Cramer2, Fredrik Haas3, Jo S. Hermansen1, Anna Runemark1,3, Arild Johnsen2 and Glenn‑Peter Sætre1 Abstract Background: Postzygotic isolation in the form of reduced viability and/or fertility of hybrids may help maintain species boundaries in the face of interspecific gene flow. Past hybridization events between house sparrows (Passer domesticus) and Spanish sparrows (P. hispaniolensis) have given rise to a homoploid hybrid species, the Italian sparrow (P. italiae). Although genetic incompatibilities are known to isolate these three species, the biological consequences of these incompatibilities are still unknown in early generation hybrids. Methods: We investigated whether F1 hybrids between house and Spanish sparrows experience reduced viability or fertility. More specifically, we generated hybrids through controlled crosses in aviaries, and compared ovaries of female hybrids with female of pure-species sparrows. Results: We found that overall, hybrid ovaries were underdeveloped and that half of all female hybrids exhibited symptoms of ovarian hypofunction (ovarian atrophy and complete absence of developed follicles). Conclusions: Fertility in hybrids is a common consequence or post-zygotic barriers between species. We discuss these results in light of previous findings on genetic incompatibilities between the parent species and the potential role of incompatibilities in hybrid speciation, a rare evolutionary process in birds. Keywords: Hybrid fitness, Hybridization, Ovary, Sparrows, Speciation Background mechanisms may constrain or facilitate hybrid specia- As divergence in allopatry between two species increases, tion (Abbott et al. 2013; Schumer et al. 2014). It has been levels of postzygotic isolation are also likely to increase hypothesized that postzygotic barriers may hinder the (Coyne and Orr 1997). Extrinsic sources of postzygotic hybrid speciation process as they will, by necessity, isolation, when hybrids are ecologically or biologically involve the purging of genetic incompatibilities in early unfit, are thought to play an important role in the early generation hybrids (Nolte and Tautz 2010). However, if stages of population divergence, while intrinsic genetic instead these incompatibilities can be sorted in such a incompatibilities causing hybrid sterility and/or invi- way that one subset of the genes function as reproductive ability are thought to develop later (Presgraves 2010; barriers against one of the parents and a different sub- Seehausen et al. 2014). However, little is known about set against the other parent (Trier et al. 2014), they may postzygotic isolation between pairs of species for which favor the emergence of a fully isolated new hybrid lineage past hybridization has generated a new species that is (Hermansen et al. 2014; Trier et al. 2014). reproductively isolated from both parents (a process The house sparrow (Passer domesticus) and Spanish called hybrid speciation; Mallet 2007). Such informa- sparrow (P. hispaniolensis) are two closely related, eco- tion is critical if we want to understand which isolating logically similar passerine species. However, differences in habitat and timing of breeding appear to represent *Correspondence: [email protected] pre-mating barriers to gene exchange (Summers-Smith 1 Department of Biosciences, Center for Ecological and Evolutionary 1988; Hanh Tu 2013). In contrast, there is currently no Synthesis, University of Oslo, PO Box 1066, Blindern, 0316 Oslo, Norway Full list of author information is available at the end of the article evidence for post-mating prezygotic isolation (Cramer © 2016 Eroukhmanoff et al. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons. org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Eroukhmanoff et al. Avian Res (2016) 7:3 Page 2 of 5 et al. 2014). Past episodes of hybridization between 4 Spanish sparrows) and inspected their reproductive house sparrows and Spanish sparrows have resulted in organs. All birds were mature adults (i.e. at least 2 or more the formation of a homoploid hybrid species, the Italian years of age, either wild caught or aviary-born) and had sparrow (P. italiae) (Elgvin et al. 2011; Hermansen et al. been maintained in captivity under identical conditions for 2011). Further, the two parent species are still sympatric at least two years prior to the current experiment. in many parts of their range and occasionally hybridize Prior to dissection, we measured tarsus length and (Summers-Smith 1988; Hermansen et al. 2014). There is beak height with a caliper to the nearest 0.1 mm, wing also molecular evidence that these two species are iso- length with a ruler to the nearest 0.5 mm, and body mass lated by Z-linked genetic incompatibilities (Hermansen with a Pesola balance to the nearest 0.1 g. Ovaries from a et al. 2014). However, little is known about the biologi- total of 18 adult females were scored as either normally cal consequences of these genetic incompatibilities and developed or atrophied (the main symptom of ovarian whether they are of an extrinsic and/or intrinsic nature. hypofunction) and stored in RNA-later buffer for future Haldane’s rule predicts that the heterogametic sex transcriptomic work. We measured length and width for should suffer more from genetic incompatibilities (Hal- each ovary with a digital caliper to the nearest 0.1 mm dane 1922). In birds, the female is the heterogametic sex and calculated their volume based on the assumption (ZW) and is hence predicted to suffer more from intrin- that ovaries are ellipsoids with equal height and width. sic incompatibilities than male hybrids. Here, we inves- We also inspected each ovary for the presence of prehi- tigate whether hybrid females between house sparrows erarchal follicles and counted the number of pre-ovula- and Spanish sparrows exhibit reduced fertility (through tory follicles if any were present. We took photographs of ovarian hypofunction indicated by ovarian atrophy and/ one normally developed ovary from a pure house spar- or complete lack of follicular development) by dissecting row female and one atrophied ovary from an F1-hybrid and measuring the ovaries from experimental interspe- female (cross between a house sparrow sire and a Span- cific crosses between these species. ish sparrow dam). We performed an ANOVA to test for significant differences in ovary volume between hybrid Methods and pure-species females and also between species. We We used captive populations of the two species to form also investigated whether the ovary width or length of experimental crosses in a common garden environment. some hybrid females (i.e. those that exhibited atrophied We captured house sparrows in Oslo, Norway (59.934°N, ovaries) were significant statistical outliers compared to 10.723°E), and Spanish sparrows in Badajoz, Spain the distribution of pure-species ovary widths or lengths (38.649°N, 7.215°W); most birds were captured in 2010, using the Z-score method. A Fisher’s exact test was per- and breeding activity was monitored the following years. formed to determine whether the proportion of individu- Sparrows were maintained in mixed-sex aviaries hous- als with ovarian hypofunction was elevated in hybrids ing 15–18 pairs of birds. Although there is no known relative to pure individuals. Furthermore, to investigate information about the pedigrees of these different avi- whether potential differences in follicle development aries for logistic reasons, inter and intraspecific crosses between normal and potentially atrophied ovaries were were controlled through the following design: two aviar- not only physical but also functional, we used an ANOVA ies contained males and females from a single species, to test for species and hybrid differences in the number of while two other aviaries contained males from one spe- pre-ovulatory follicles. We then conducted a one sample cies and females from the other species. Hence, hybrids t test to determine whether the average number of pre- sired from both types of parental combinations, as well ovulatory follicles found in normal ovaries, irrespective as pure house and Spanish sparrows, were generated in a of species, was significantly different from 0 (the number controlled fashion. found in all atrophied ovaries). The birds were fed ad libitum with seeds and dried insects, and were supplemented with mealworms during Results the breeding season. We provided nest boxes and nesting All individuals in the study had morphological features material and allowed the birds to breed and pair without within their respective species ranges: F1 hybrids did not interference. A number of birds in all four aviaries bred differ from either parent species in tarsus or wing length, successfully, and eggs were laid between April and Septem- beak height or body mass (Table 1). However, on average, ber each year. During
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