Kin Signatures Learned in the Egg? Red-Backed Fairy-Wren Songs Are Similar to Their Mother's In-Nest Calls and Songs

Abstract

Many vocal animals recognize kin using vocal cues, in territorial contexts and in rearing young, but little is known about the developmental and evolutionary mechanisms that produce vocal kin recognition systems. In the cooperatively breeding red-backed fairy-wren (Malurus melanocephalus), females give specific "in-nest calls" while incubating their eggs. Elements from these calls are incorporated into chicks' begging calls, and appear to be used by parents for recognition. This is likely a result of an embryo's ability to learn the call elements in the egg. Here, we explore the idea that maternal vocal elements may be incorporated into offspring's adult songs, and serve as signatures of kinship, which would aid in kin recognition and benefit signaler and receiver. To investigate this hypothesis, we tested for similarities between maternal vocal elements (in-nest calls and songs) and songs of their adult offspring. We then determined whether offspring songs were more similar to the maternal vocalizations they heard only as embryos (in-nest calls), or maternal songs they heard throughout development, but mostly post-fledge (mothers' full songs). We used dynamic time warping to compare maternal vocal elements with elements in their offspring's adult songs. The elements of each offspring were more similar to the elements of their own mother than to the elements of any other female (but only for the average similarity score), suggesting they may serve as kin signatures. We also found that offspring song elements were more similar to their mother's song elements than to their mother's in-nest call elements. In addition, female in-nest call elements were more similar to their own song elements than to the song elements of any other female. Offspring that produced song elements highly similar to their mother's song elements also had song elements highly similar to their mother's in-nest call elements. Signals of kinship may function critically for survival and successful reproduction, by allowing an individual to allocate care and defense to kin and to avoid mating with genetic relatives. Understanding the processes that facilitate effective kin recognition, including development of kin signatures, helps us to understand how these crucial signaling systems may have evolved.

Kith or Kin? Familiarity as a Cue to Kinship in Social Birds

“…In practice, it is extremely difficult to rule out prior association in most field studies, even in cross-fostering experiments where there is often a period of association between parents and offspring prior to separation (e.g., Hatchwell et al, 2001). Kin recognition cues may even develop during gestation (e.g., Hepper, 1987) or incubation (e.g., Colombelli-Négrel et al, 2012;Dowling et al, 2016). Secondly, familiarity is generally assumed to result in dichotomous classification of conspecifics into familiar (kin) and unfamiliar (non-kin) individuals, while cue-template similarity under phenotype-matching is assumed to be continuous.…”

Prenatal exposure to incubation calls affects song learning in the zebra finch

“…Accordingly, a recent study in superb fairy-wrens ( Malurus cyaneus ) suggested that embryos responded to males’ (but not females’) songs, as indicated by changes in embryonic heart rate 6 . Likewise, in the closely-related red-backed fairy-wren ( M. melanocephalus ), a correlational study found that individuals’ adult song partly resembled their mother’s song, which in turn had similarities with her incubation call 16 . This raises the possibility that prenatal incubation call exposure might, indeed, bias individuals towards learning particular songs later in life, although this remains to be tested.…”

How frequent and important is behavioral thermoregulation by embryonic reptiles?

“…They sometimes exhibit specific morphological adaptations to do so (e.g., teeth in caecilian embryos: Wake, ); Kill siblings to reduce competition for food —for example, invertebrates (Harrath, Sluys, Zghal, & Tekaya, ; Thomsen, Collin, & Carrillo‐Baltodano, ) and sharks (Gilmore, ); Regulate amniotic fluid volume by drinking —Cordero et al. () interpret sucking behavior pre‐birth as nonfunctional, but this behavior plausibly adjusts fluid volumes among compartments of the oviductal package (i.e., moving fluid from the amniotic sac to the allantois), thereby enhancing offspring viability (El‐Haddad, Desai, Gayle, & Ross, ); “Eavesdrop” on developmental rates of siblings —enabling embryos to hatch synchronously with the rest of the clutch, thereby gaining fitness benefits associated with concurrent emergence from the nest, predator satiation, and so on (McGlashan, Spencer, & Old, ); Identify the optimal time to hatch based on external cues —including diel cycles (Radder & Shine, ), drought stress (Newman, ), and imminent predation (Warkentin, ); Learn dialect of local songs —by listening to the mother's vocal repertoire while they are still inside the egg (in birds: Dowling, Colombelli‐Négrel, & Webster, ); Vocalize within the egg shortly before hatching —to induce hatching in siblings and stimulate the adult female to open the nest (in crocodilians: Vergne & Mathevon, ) or to exhibit other parenting behaviors (in birds: Bolhuis & van Kampen, ; Reed & Clark, ; Rumpf & Nichelmann, ); and Reposition within the egg —to behaviorally thermoregulate (reptiles: Du et al., ; birds: Li et al., ; Marasco & Spencer, ).…”

“…Learn dialect of local songs —by listening to the mother's vocal repertoire while they are still inside the egg (in birds: Dowling, Colombelli‐Négrel, & Webster, );…”