biology

big little liars , mimicry and speciation in the indigobirds and whydahs of

Text gabriel a. jamie

It’s the start of the rains in southern and a small, glossy black is singing incessantly from the top of an exposed tree. The song is mostly a hurried ramble of chatters and scratchy warbles, but occasionally the intersperses trills and tinkling notes that sound nearly identical to those of a lo- cal of . This seemingly inconsequential observation hints at a fascinating evolutionary story unfolding in woodlands and savannas throughout Africa.

he finch is an indigobird, a member of the family that also includes the whydahs andT Finch. As the latter’s name suggests, the family’s reproductive be- haviour shares similarities with that of many . Rather than constructing a nest, incubating eggs and feeding young, they adopt a ‘brood-parasitic’ lifestyle, depositing their eggs in the nests of other and letting them do all the work. As strategies go, it’s a good one. Rear- ing offspring is a time-consuming and energy-intensive endeavour. While off- spring are young and unable to care for themselves, parents must return fre- quently to the nest site to bring food, carry out nest maintenance and defend their chicks from predators. This se- warwick tarboton verely curtails the adult’s mobility and parental care, they free up time and en- A male Long-tailed Paradise Whydah increases its own susceptibility to attack. ergy for producing more eggs. These (opposite) surveys his territory. As a nestling, What’s more, the adult literally has all eggs can then be spread across many this bird would have grown up in the nest of its eggs in one basket. If something goes host nests rather than being concentrat- a Green-winged (above). wrong at any stage in the process, its re- ed in a single one. This distributes risk productive output is completely lost and and means that even if one of the nests tied to a single nest site and having com- its efforts wasted. gets preyed upon, the parasite’s entire re- mitted the parasitic act they are free to Brood parasites, in contrast, have productive output is not compromised. move as other pressures, such as food, no such constraints. By outsourcing The adult parasite’s movements are not moult and weather, dictate. >

Tertius A. Gous january/february 2021 BROOD PARASITES 35 An adult male (above). This that make the parasite’s job much harder. All indigobirds and whydahs are spe- bird would have been raised in the nest of its These include mobbing adult parasites cialised brood parasites on species in the specialist host, Jameson’s Firefinch (opposite). seen near the nest and removing odd- grassfinch family (). There looking eggs or chicks that could have are 10 indigobird species and nine why- warwick tarboton (2) However, despite the apparent benefits come from another species. dahs currently recognised. Indigobirds family or why it is so diverse yet species- The Estrildidae are excep- humans, allowing them to perceive ultra- of a parasitic lifestyle, less than one per Even if hosts lack these defences, not mostly parasitise and twin- specific. Parasitism byVidua alone can- tional in that, unlike the violet light. Moreover, nestling begging cent of the world’s bird species exclu- all are suitable candidates for parasitism. spots, while the hosts of whydahs are not account for it, as many estrildid finch nestlings of most birds displays involve multiple dimensions, in- sively adopt it. Globally, obligate brood Some have nest entrances that would be generally and waxbills. Unlike species in Asia and Australasia, beyond corporating not just visual but vocal and that are cryptically parasitism is thought to have evolved too small for the adult parasite to enter most other avian –host the range of , have such ornamen- postural components too. These, it turns independently seven times in birds, with or the fledgling parasite to leave, while relationships, in which the interacting tation too. patterned, estrildid young out, are as diverse and species-specific three separate origins among cuckoos others feed their young the wrong type parties are often much more distantly However, we do know that the col- boast the most elaborate across the Estrildidae as their mouth and one each in the , cow- of food. Taken together, this means that related, the Viduidae and Estrildidae ours and patterns of each estrildid spe- and diverse appearances of markings. Does Vidua mimicry extend birds and parasitic . Even a some- the range of possible hosts occurring at a are sister families thought to share a cies are important in ensuring parents any bird family in the world into these modalities too? what anomalous duck in South America given locality for a given parasite can be common ancestor around 10 to 15 mil- feed them adequately. When the mouth It was in this context that I, together has gone down this route. But why don’t quite small. The parasite may then itself lion years ago. markings of nestling estrildid finches by the foundational research of Jürgen with Claire Spottiswoode and other col- more bird species implement the strat- have to evolve specialised adaptations to The Estrildidae are exceptional in are altered slightly, they are fed less by Nicolai and Robert Payne. However, leagues, conducted research on the Vidua egy? One possibility is that while being a circumvent host defences. While these that, unlike the nestlings of most birds parents than those with ‘normal’, un- while these studies laid the foundation radiation. We set out to quantitatively test parasite avoids certain problems, it gen- adaptations make the parasite effective that are cryptically patterned, estrildid manipulated markings. This suggests for our current understanding of the whether Vidua nestlings truly do mimic erates a whole set of new ones. at exploiting one host, they can equally young boast the most elaborate and di- that, in order to convince host parents Vidua finch radiation, methodologi- the appearance, sounds and movements The challenges of being a parasite be- make it poorly suited to another. As verse appearances of any bird family in to feed them enough food, Vidua nest- cal limitations at the time meant that of their host nestlings. The first step, come apparent when one realises that parasites become specialised on a small the world. Some have an almost other- lings need to have similar mouth mark- the existence of this mimicry could not however, was to find a parasitised nest! hosts are not passive and willing par- number or even a single host, they be- worldly appearance, with luminous ings to those of their host. be tested in a systematic or quantitative This was easier said than done, but over ticipants, eager to have the role of foster come dependent on that species and are papillae lining the gape and complex manner, nor tested from a bird’s perspec- five years of field work at our study site parent foisted upon them. From an evo- vulnerable if it goes locally extinct. combinations of spots and bars adorning Nestling mimicry by Vidua tive. Subjective human assessments are near Choma, southern Zambia, together lutionary perspective, the host’s effort the palate. These patterns vary widely finches not necessarily good proxies for simi- with Collins Moya, Silky Hamama and in rearing the distantly related young of The Vidua finches between estrildid species but little within The idea thatVidua nestlings may larity as perceived by birds, since birds a team of skilled nest-finding assistants, another species is entirely wasted and This brings us back to our seemingly them, making them highly character- mimic the appearance, and particularly process colour and pattern differently we managed to find parasitic chicks of diverts investment away from its own innocuous indigobird singing ebul- istic of each. It is not yet understood the mouth markings, of their specific to humans. For instance, many birds three Vidua species: the Pin-tailed Why- offspring. Many hosts have therefore liently in the midday heat of southern what evolutionary pressures led to the estrildid host goes back to the work of have four colour-receptive cones in their dah, Broad-tailed Paradise Whydah and evolved a suite of defensive strategies Zambia. origin of nestling ornamentation in this Robert Neunzig and was later extended retina, as opposed to just three in most Purple Indigobird. >

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more precise mimicry to have evolved or because current levels of mimicry are already good enough to fool the host par- ents. Some imperfections might actually be enhanced versions of the host’s signal, stimulating it to feed the parasite chick even more than it would its own chicks, though this hypothesis remains untested at present.

Vocal imitations of hosts by adult Vidua That some of the adult indigobird’s vo- calisations resemble those of a firefinch is not coincidental. It stems from the ca- pacity that many Vidua finches have to imprint on their hosts, as uncovered by a species. Male song and female host and The author’s set-up to photograph inside the series of detailed and painstaking experi- mate preferences develop differently de- mouths of nestling birds. ments by Robert Payne and colleagues. pending on the host species they are raised Specifically, male Vidua learn the song by. If a female accidentally lays her eggs in sanguinidorsalis and its association with of the host species in the nest and grow the nest of a new host species, her sons the Vidua maryae. up to incorporate elements of the host’s will sing like the new host. Her daughters The extent to which new ‘host races’ of vocalisations in their own display to at- will grow up to be attracted to males who Vidua are necessarily new species is de- tract mates. Therefore, males broadcast to sing like the new host, as well as to prefer- batable and it has been suggested that as females the identity of the host they were entially parasitise that new host. This has well as being imprinted on the new host, raised by. Incidentally, they also broadcast the potential to initiate a new lineage of it should also be proven that the nestling this information to attentive birders, pre- Vidua that is reproductively isolated from of that Vidua species has mouth mark- senting a unique opportunity in the study the Vidua specialising on the traditional ings that mimic those of the host. Thus, of brood-parasitic birds whereby patterns host. Such new, reproductively isolated the gold standard for a new Vidua spe- of host use can be ascertained purely by lineages are, at least according to some cies requires proving both that the adult sound recording rather than DNA ana­ species concepts, the very definition of male imitates the song of the new host lysis or nest finding. Many Vidua species, newly formed species. Detailed work on and that the nestlings mimic the begging particularly indigobirds, are extremely the genetics and evolutionary relation- displays. The nestlings of finches in the family Estrildi- To test for visual mimicry, we de- species receiving these begging signals similar to one another in appearance. ships among Vidua by Michael Sorenson Finally, it should be noted that the dae are unusual in having very diverse and veloped a method of photographing (that is, the host parents). Listening and recording the male’s song and colleagues supports this mode of spe- imprinting mechanism not only pro- elaborate mouth markings. These images inside the mouths of Vidua nestlings. We showed that for at least the three to identify which host they are imitating ciation. Thus, in Vidua, the shift to a new motes speciation, but also has the po- illustrate some of the diversity in nestling ap- With the help of Jolyon Troscianko, we species of Vidua we studied, the nestling is often the best way to identify them, es- host and the formation of new species are tential to generate hybridisation. If a pearance that exists between species. The top came up with a system in which the parasites do indeed mimic the mouth pecially in parts of where the intricately connected. female Vidua lays in the nest of a host two rows show the insides of the mouths of chick was held below a prism until its markings (both colour and pattern) of genus reaches its peak diversity. Therefore, if an observer finds an species already exploited by another Figure 1 various species of nestling estrildid finch. The mouth opened naturally. We then gen- their hosts. In addition, we found that The capacity to imprint on hosts is not indigobird imitating a previously un- lineage of Vidua, the offspring of the bottom row shows recently hatched chicks tly pressed the mouth over the apex of they mimic the begging calls and postural limited to Vidua males. Females do it known host, it is possible that they will two lineages will now share a common of three estrildid finch species. Many of these the prism. This allowed the angular in- movements of their hosts when begging. too, but for them it is their mate and host have discovered a species of indigobird song (males) and mate/host prefer- species are hosts to indigobirds and whydahs. terior surfaces of the chick’s mouth to The mimicry seems to be genetically en- preferences that are guided by their early that is new to science. Recent discover- ence (females). This sets the stage for Top row, left to right: Locust Finch, Common be projected at a consistent angle onto coded rather than learned, because when life experiences. A female Vidua grows ies of novel Vidua hosts include Dusky lineages to collapse as mating now oc- Waxbill, Blue Waxbill, Green-winged Pytilia, the prism face opposite this edge, which we moved parasite eggs into a new host up to be attracted to males who sing like Twinspot in , Pink-throated curs freely across previously isolated Orange-winged Pytilia. Middle row, left to could then be photographed with a spe- species’ nest and let them grow there, the same host she was raised by and to Twinspot in KwaZulu-Natal, Brown groups. Hybrid Vidua are occasion- right: Red-billed Firefinch, Jameson’s Firefinch, cially modified camera that could detect they did not develop begging displays to deposit her eggs in the nest of the same Firefinch in southern Zambia and Black- ally observed and genetic studies sug- Zebra Waxbill, African , Bronze ultraviolet light as well as human-visible match those of the new host but retained species as she was raised by. crowned Waxbill in . A new gest that there is often continuing gene Mannikin. Bottom row, left to right: Green- wavelengths of light. The colours and those of their ancestral host. species of firefinch was even discovered flow between Vidua lineages special- winged Pytilia, Red-billed Firefinch, Locust patterns obtained from these images Despite the astonishing intricacy and Imprinting and the origin of in by the sound recording of an ised on different hosts. The possibility Finch. All photos by Gabriel A. Jamie except were then processed through models of specificity of the mimicry, we did find new Vidua species indigobird imitating the call of an un- of hybridisation as a source for novel Green-winged Pytilia at bottom left by Claire avian vision, en­abling us to assess the some minor imperfections. These may This imprinting mechanism has conse- known firefinch. This led to the discov- mimicry adaptations to host nestlings N. Spottiswoode. mimicry in a way that is relevant to the exist as a result of insufficient time for quences for the formation of new Vidua ery of the Lagonosticta remains to be explored. >

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Host 1 Parasite 1 Host 2 Parasite 2 Host 3 Parasite 3 evolving mimicry of the mouth mark- Parasite–host relationships in the Vidua finches. Modified from Sorenson et al. 2004, Host 1 Parasite 1 Host 2 Parasite 2 Host 3 Parasite 3 Broad-tailed Systematic Biology. Primary host indicated by asterisk * Common waxbill Pin-tailed whydah Orange-winged pytilia Jameson’s firefinch Purple indigobird ings, begging calls and head movements Common Waxbill Pin-tailed Whydah Orange-winged Pytilia Broad-tailedparadise Paradise whydah Whydah Jameson’s Firefinch Purple Indigobird Estrilda astrild Vidua macroura Pytilia afra Lagonosticta rhodopareia Vidua purpurascens Estrilda astrild Vidua macroura Pytilia afra ViduaVidua obtusaobtusa Lagonosticta rhodopareia Vidua purpurascens of their hosts. Vidua species Host species The ability to switch from one host to 1.0 V. chalybeatea *Red-billed Firefinch Lagonosticta senegala another is likely to be easier when the L. nitidula nestlings of the old and new host spe- Zambezi Indigobird V. codringtoni *Red-throated Twinspot Hypargos niveoguttatus 0.8 cies have more similar begging displays. Pink-throated Twinspot H. margaritatus This allows adaptations to the old host V. funerea * L. rubricata 0.6 to be at least partially successful in the new host. Over generations, we could Dusky Twinspot Euschistospiza cinereovinacea imagine that such rudimentary mimicry Purple Indigobird V. purpurascens Jameson’s Firefinch L. rhodopareia Proportion 0.4 Proportion can be refined by natural selection to Baka Indigobird V. larvaticola *Black-faced Firefinch L. larvata produce more accurate mimicry. More Firefinch L. virata 0.2 closely related hosts have more simi- Jos Plateau Indigobird V. maryae Rock Firefinch L. sanguinodorsalis lar begging displays and this probably Wilson’s Indigobird V. wilsoni Bar-breasted Firefinch L. rufopicta explains the phenomenon that, when 0.0 V. camerunensis *Black-bellied Firefinch L. rara Vidua do switch to a new host, it is of- *African Firefinch L. rubricata ten one that is in the same genus as the Dybowski’s Twinspot E. dybowskii old one. Research on the evolutionary Brown Twinspot Clytospiza monteiri relationships of both Vidua and estrildid Quailfinch Indigobird V. nigeriae African Quailfinch Ortygospiza atricollis finches by Michael Sorenson and col- leagues supports this pattern, which has V. raricola Zebra Waxbill Amandava subflava Shaft-tailed Whydah V. regia Violet-eared Waxbill granatina Photographs by Gabriel A. Jamie. Illustrations reproduced with kind been termed ‘clade-limited colonisation’. permission of Faansie Peacock. Figure from Jamie et al. 2020, Evolution. Several factors probably constrain the Straw-tailed Whydah V. fischeri G. ianthogaster Figure 2 colonisation of new hosts and therefore Steel-blue Whydah V. hypocherina Black-faced Waxbill Estrilda erythronotos above Nestlings of many indigobirds and why- Conclusion however, due to the unique combina- the formation of new Vidua species. Black-cheeked Waxbill E. charmosyna dahs mimic the appearance, begging calls and Taken together, our current understand- tion of appearance, calls and movements Firstly, habitat; Vidua generally avoid Pin-tailed Whydah V. macroura *Common Waxbill E. astrild movements of their respective hosts. The top ing of the Vidua radiation can be sum- made by each species’ young. A key rainforest and consequently do not para- *Orange-cheeked Waxbill E. melpoda row shows photographs of the mouth markings marised as follows: barrier to host switching, and therefore sitise any of the estrildids that inhabit it. *Black-rumped Waxbill E. troglodytes of three pairs of hosts and parasites that the Speciation and host switching are in- speciation, seems to be persuading host Secondly, some estrildid species have *Red-rumped Waxbill E. rhodopyga author collected data on in southern Zambia: timately linked due to the capacity of parents to feed them adequate amounts mouth markings too dissimilar from *Fawn-breasted Waxbill E. paludicola 1) Common Waxbill and Pin-tailed Whydah, Vidua to imprint on their host parents, of food rather than the right kind of food other already parasitised species to allow *Swee Waxbill Coccopygia melanotis 2) Orange-winged Pytilia and Broad-tailed which alters male song and female mate/ (DNA barcoding suggests little variation Vidua to easily switch. Examples include East African Swee C. quartinia Paradise Whydah and 3) Jameson’s Firefinch host preferences. Each estrildid finch in nestling diet among estrildid finches the mannikins ( species) and Bronze Mannikin Spermestes cucullata and Purple Indigobird. The top row shows presents its own challenge to parasitise, in an area). Vidua overcome this by the Locust Finch Paludipasser locustel- Zebra Waxbill A. subflava photographs of the mouth markings of nest- la, both of which have a distinct bar on Blue Waxbill angolensis lings of each species. You can see how closely the upper palate that no Vidua has yet Long-tailed Paradise Whydah V. paradisaea Green-winged Pytilia Pytilia melba the parasite mimics the colours and patterns evolved to mimic. It is likely that the com- Broad-tailed Paradise Whydah V. obtusa Orange-winged Pytilia P. afra of its host’s nestlings. The second row shows bination of these factors has limited the V. orientalis Green-winged Pytilia P. melba the pattern of black markings on the inside Vidua radiation to its current extent of Exclamatory Paradise Whydah V. interjecta *Red-winged Pytilia P. phoenicoptera of the upper palate of each species. Again you 19 species, rather than having diversified Yellow-winged Pytilia P. hypogrammica can see how closely the patterns inside the much further by exploiting the full range Red-faced Pytilia P. lineata mouth of the parasite matches that of its of estrildid finches occurring in Africa. Paradise Whydah V. togoensis Yellow-winged Pytilia P. hypogrammica host. The third row shows sonograms of the Given the specialised nature of Vidua– begging calls of each species; the similarity host relationships, it will be fascinating to in call structure between each species is clear. see to what extent changes in host distri- could set the stage for new host switches Cape Town. His research on mimicry and The bottom row shows adult males of each butions in the coming decades driven by and the start of fresh cycles of speciation, speciation in Vidua finches was supported species. climatic changes and bush encroachment hybridisation and mimicry.  by a research project grant from The Lev- are matched by changes in the distribu- erhulme Trust. To find out more about right A nestling Purple Indigobird (right) tions of their respective parasites. Simi- Gabriel Jamie is a postdoctoral researcher the work of the research group, visit www. that was being raised with two Jameson’s larly, shifting ranges of estrildid finches at the University of Cambridge and a re- africancuckoos.com. If you would like Firefinch chicks (left). The similarity in mouth may bring previously unparasitised spe- search associate at the FitzPatrick Institute more information about Vidua finches, markings between the species is evident. cies into contact with Vidua. This in turn of African Ornithology at the University of contact the author at [email protected] Claire N. Spottiswoode

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