Sharp acoustic boundaries across an altitudinal avian hybrid zone despite asymmetric introgression

Abstract

Birdsong is a sexually selected trait that could play an important evolutionary role when related taxa come into secondary contact. Many songbird species, however, learn their songs through copying one or more tutors, which complicates the evolutionary outcome of such contact. Two subspecies of a presumed vocal learner, the grey-breasted wood-wren (Henicorhina leucophrys), replace each other altitudinally across the western slope of the Ecuadorian Andes. These subspecies are morphologically very similar, but show striking differences in their song. We examined variation in acoustic traits and genetic composition across the altitudinal range covered by both subspecies and between two allopatric populations. The acoustic boundary between the subspecies was found to be highly abrupt across a narrow elevational range with virtually no evidence of song convergence. Mixed singing and use of hetero-subspecific song occurred in the contact zone and was biased towards the use of leucophrys song types. Hetero-subspecific song copying by hilaris and not by leucophrys reflected a previously found asymmetric pattern of response to song playback. Using amplified fragment length polymorphisms (AFLP) markers, we detected hybridization in the contact zone and asymmetric introgression in parapatric populations, with more leucophrys alleles present in hilaris populations than vice versa. This pattern may be a trail of introgression due to upslope displacement of leucophrys by hilaris. Our data suggest that song learning may impact speciation and hybridization in contrasting ways at different spatial scales: although learning may speed up population divergence in songs, thereby enhancing assortative mating and reducing gene flow, it may at a local level also lead to the copying of heterospecific songs, therefore allowing some level of hybridization and introgression.

Behavioural response to song and genetic divergence in two subspecies of white‐crowned sparrows (Zonotrichia leucophrys)

“…Halfwerk et al . ). In comparison, concordance between symmetrical song discrimination and secondary contact with reduced gene flow would suggest song acting as a behavioural barrier.…”

“…If evidence of asymmetric gene flow between taxa coincides with a pattern of asymmetric recognition of songs, then this pattern would provide support for song as an incomplete behavioural barrier (e.g. Halfwerk et al 2016). In comparison, concordance between symmetrical song discrimination and secondary contact with reduced gene flow would suggest song acting as a behavioural barrier.…”

“…Halfwerk et al . ), songs are often more convergent in sympatry, due to local acoustic adaptation or interspecific learning (Secondi et al . ; Haavie et al .…”

“…Although studies of hybridizing lineages typically find song divergence in allopatry (e.g. Halfwerk et al 2016), songs are often more convergent in sympatry, due to local acoustic adaptation or interspecific learning (Secondi et al 2003;Haavie et al 2004;Qvarnstr€ om et al 2006;Kenyon et al 2011), or hybridization itself (de Kort et al 2002). Likewise, in many cases, individuals in hybrid zones discriminate between diverged songs (Patten et al 2004;Tur cokov a et al 2011;Greig & Webster 2013), while in other cases, individuals do not discriminate between nonlocal and local songs (Matessi et al 2000;Gee 2005;den Hartog et al 2008), or there is asymmetric song recognition (Kershner & Bollinger 1999;Dingle et al 2010;Ruegg et al 2012;McEntee 2014;Pegan et al 2015).…”

Origin of elevational replacements in a clade of nearly flightless birds – most diversity in tropical mountains accumulates via secondary contact following allopatric speciation

“…A promising additional case is that of Syma kingfishers in New Guinea, in which two distinct species co-occuring with elevational segregation have experienced gene flow yet maintain divergence in regions of the genome likely involved in adaptation and, presumably, mate choice (Linck et al, 2019). In contrast to the Senecio and Syma examples, avian taxa replacing each other with elevation in Neotropical mountains seldom show evidence of gene flow, with the only documented cases of interbreeding between elevational replacements in the region we are aware of being those of Anairetes tit-tyrants in Peru (Dubay & Witt, 2014), Myiarchus flycatchers in Bolivia (Lanyon, 1978), Henicorhina wood-wrens in Ecuador (Halfwerk et al, 2016), and Ramphocelus tanagers in Colombia (Sibley, 1958;Morales-Rozo et al, 2017). The apparent paucity of hybridization between birds replacing each other with elevation in the Neotropics further suggests that elevational replacements did not originate through primary divergence in parapatry in the absence of barriers to gene flow, but instead via secondary contact of reproductively isolated populations.…”