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Insect Systematics and Diversity, (2019) 3(4): 1; 1–5 doi: 10.1093/isd/ixz008 Short Communication Short Communication

Implications of a Dating Analysis of Hippoboscoidea (Diptera) for the Origins of Phoresis in Feather Lice (Psocodea: Phthiraptera: )

Robert S. de Moya1,2,3

1Department of Entomology, University of Illinois Urbana – Champaign, 505 S. Goodwin Ave., Urbana, IL 61801, 2Illinois Natural Downloaded from https://academic.oup.com/isd/article/3/4/1/5525310 by guest on 24 September 2021 History Survey, Prairie Research Institute, University of Illinois Urbana – Champaign, Champaign, IL 61820, and 3Corresponding author, e-mail: [email protected]

Subject Editor: Brian Wiegmann

Received 15 January, 2019; Editorial decision 4 June, 2019

Abstract (Samouelle 1819) is a family of blood feeding Diptera, which can be phoretic vectors for para- sitic feather lice (Philopteridae Burmeister 1838). Hippoboscid are understood to provide opportunities for increased instances of dispersal and host-switching for feather lice. This intimate relationship between hippoboscid and feather may have hypothetically existed since the origin of avian-specialized Hippoboscidae. Thus, phoretic dispersal may have affected patterns of diversification in feather lice over millions of years. To test this, a dating analysis of a previously published Hippoboscoidea data set was per- formed using known fossil calibrations. The results of the dating analysis suggest Hippoboscoidea diversified shortly after the K-Pg boundary, similar to their modern vertebrate hosts. A maximum age of the avian feeding Ornithomyini is estimated to have occurred around the origin of parasitic feather lice. This maximum diver- gence date suggest this phoretic relationship could have existed for much of the diversification of avian feather lice and had the potential to influence patterns of diversification due to dispersal and host-switching among avian hosts.

Keywords: Hippoboscoidea, Hippoboscidae, Philopteridae, phoresis, Phylogenetics

Hippoboscidae (Samouelle 1819) (louse flies) is a family of ectopara- was such a common occurrence that no records were kept in the sitic Diptera that feeds on the blood of mammals and birds (Maa ensuing years” (Bennett 1961). 1969). Although, they are conspicuous parasites that most ento- Phoretic attachment to various Diptera has been reported in sev- mologists are familiar with, few appreciate the impact these flies may eral major groups of parasitic lice (Phthiraptera), but the morph- have had on the evolution of another group of . Numerous ology used for attachment to the fly varies among lineages (Keirans reports exist of phoretic feather lice (Philopteridae Burmeister 1975, Price et al. 2003, Bartlow et al. 2016). For example, mem- 1838) attached to hippoboscid flies which share a common avian bers of Philopteridae are known to grasp onto passing hippoboscids host (Markov 1938, Corbet 1956, Bennett 1961, Keirans 1975, using mandibles that move in a dorsoventral axis perpendicular to Macchioni et al. 2005, Harbison et al. 2009, Bartlow et al. 2016). the head which allows the space required for attachment. However, This phoretic relationship is thought to provide a mechanism for the mandibles of move in a parallel plane to the ven- host-switching among potential avian hosts in an ecosystem (Price tral surface of the head, which inhibits phoretic attachment (Keirans et al. 2003). Thus, hippoboscid flies have the potential to influence 1975, Price et al. 2003). Phoresis also occurs in the Anoplura the evolution of feather lice by allowing for increased instances of (sucking lice) but this group lacks chewing mandibles for attach- dispersal and host-switching among distantly related bird species, ment. Sucking lice may also prefer (house flies) as phoretic which can result in cophylogenetic incongruence between parasite vectors but phoresis for sucking lice is rarely reported (Kirk-Spriggs and host topologies (Johnson, Adams, et al. 2002, Weckstein 2004, and Mey 2014, Bartlow et al. 2016). The morphology that facili- Bush et al. 2016). This phoretic relationship has been reported often tates attachment of parasitic feather lice to hippoboscid flies and rec- in the literature. One study found 68 of 156 flies sampled had phor- ords of feather louse phoresis suggests the potential for an impact of etic feather lice attached (Corbet 1956). Another study reports 41 of hippoboscid flies on feather louse evolution (Markov 1938, Corbet 180 flies possess attached feather lice and state in the text “Phoresy 1956, Bennett 1961, Keirans 1975, Bartlow et al. 2016).

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2 Systematics and Diversity, 2019, Vol. 3, No. 4

The family Hippoboscidae is a member of the superfamily 2011). Final results between MCMCTree runs were visualized for Hippoboscoidea which consists of four families [Hippoboscidae, stationarity using the program Tracer1.7.1 (Rambaut et al. 2018). + (bat flies), and Glossinidae (tsetse flies)]. All of these flies are parasitic in nature but have varying levels of interactions with their hosts (Petersen et al. 2007). A phylogenetic Results analysis of the group based on four genes revealed two host-switches The result of the maximum likelihood analysis is concordant with to birds within the Hippoboscoidea and provides the opportunity to the final phylogenetic hypothesis for Hippoboscoidea previously investigate the temporal origins of feather louse phoresis (Petersen published (Petersen et al. 2007; Fig. 1). Within the Hippoboscidae, et al. 2007). Although phylogenetic analyses provided resolution bootstrap support values are high among the groups reported as among major lineages within Hippoboscoidea, a dating analysis monophyletic [Hippoboscinae (100%), Lipopteninae (100%), was not performed. Two separate dating analyses that included Ornithomyini (100%), Olfersini (90%)]. Despite the differences Diptera more broadly suggest an origin for Hippoboscoidea of ap- in phylogenetic methodology, new analyses support the previous proximately 55–60 Mya (Wiegmann et al. 2011, Misof et al. 2014). results. However, the scope of these previous dating analyses was not fo- The results of the dating analysis suggest an origin of cused on the origins of feather louse phoresis and taxonomic sam- Hippoboscoidea to be 73 Mya (60–83, 95% HPD) and the origin of Downloaded from https://academic.oup.com/isd/article/3/4/1/5525310 by guest on 24 September 2021 pling was limited for this question. A fossil Hippoboscoidea has been true ectoparasitism (prolonged association with host) within the super- reported with an estimated age of between 30 and 40 Mya (Grimaldi family to be between 62 and 67 Mya (50–77, 95% HPD; Fig. 1). Two and Engel 2005). By integrating existing molecular data and pub- origins of avian feeding by hippoboscid flies are recovered with the lished fossil calibrations (Wiegmann et al. 2011), a dating analysis of of the historically recognized “Ornithomyiinae” (Olfersini Hippoboscoidea can be performed. and Ornithomyini; Petersen et al. 2007). The dating analysis suggests In this study, a molecular phylogenetic dating analysis was that the origin of feather louse phoresis may have occurred between 24 performed on data published for Hippoboscoidea (Petersen et al. and 52 Mya (15–63, 95% HPD) based on the divergence estimates of 2007), investigating the temporal origins of avian feeding to pro- avian specialized Hippoboscidae (Fig. 1). vide an estimate of a maximum age of feather louse phoresis. Cophylogenetic analyses of feather lice and their avian hosts have identified incongruence between parasite and host trees (Johnson, Discussion Adams, et al. 2002, Weckstein 2004, Bush et al. 2016, Sweet et al. The result of the Hippoboscoidea dating analysis suggests an origin of 2018). Growing evidence seems to indicate that host-switching may true ectoparasitism between 62 and 67 Mya near the K-Pg boundary have played a significant role in feather louse diversification relative (66 Mya). Modern bird and mammal lineages began diversifying to cospeciation processes (Johnson et al. 2018). Certain genera of after this mass extinction event (O’Leary et al. 2013, Prum et al. feather lice have been implicated in higher rates of host-switching 2015). Chiroptera (bats) are thought to begun diversifying 55.5 Mya relative to other groups and phoresis is suspected (Johnson, Adams, (O’Leary et al. 2013) and the dating analysis suggests an origin be- et al. 2002, Johnson, Weckstein, et al. 2002, Bush et al. 2016). The tween 52 and 62 Mya for bat flies. Another host that diversified diversity of feather lice which engage in phoresis may be explained following the K-Pg boundary includes the Artiodactyla (even-toed by host-switching following the origin of phoretic dispersal on ungulates; 55.8 Mya; O’Leary et al. 2013) and the dating analysis hippoboscid flies and could help explain patterns of feather louse suggests an origin of their hippoboscid parasites (Lipopteninae diversification over millions of years (Johnson, Adams, et al. 2002; + Hippoboscinae) between 39 and 43 Mya. Previous studies have Johnson, Weckstein, et al. 2002; Weckstein 2004; Johnson et al. also suggested that Neoaves began diversifying shortly following 2012, 2018; Bush et al. 2016). the K-Pg boundary (66 Mya; Prum et al. 2015).The previously com- pleted ancestral state reconstruction suggested a mammal host an- cestor within Hippoboscoidea with two host-switches to avian hosts Materials and Methods (Petersen et al. 2007) and the dating analysis suggests a host-switch Molecular data were downloaded as a PopSet (NCBI GenBank) to avian feeding may have occurred between 24 and 52 Mya (Fig. 1). (Clark et al. 2016) from a previous study on Hippoboscoidea The origin of feather louse phoresis on hippoboscid flies would (Petersen et al. 2007). The data were aligned by gene with Muscle likely have occurred between 24 and 52 Mya based on the divergence 3.8.425 (Edgar 2004) with a maximum iteration set to eight as imple- dates estimated for avian specialized Hippoboscidae. The divergence mented in Geneious 11.15 (Kearse et al. 2012). The alignments were between parasitic feather lice and other parasitic louse lineages is concatenated in SequenceMatrix100.0 (Vaidya et al. 2011) and then thought to have occurred following the K-Pg boundary (66 Mya) a maximum likelihood analysis was performed with RAxML8.2.11 with divergences among deep internodes of major feather louse lin- using a GTR+G model and 1000 bootstrap replicates (Stamatakis eages occurring approximately 60 Mya (Johnson et al. 2018). Given 2014). The resulting topology was used for a subsequent dating ana- the deep divergence within Hippoboscidae, it appears that louse lysis performed using relaxed-clock methods in MCMCTree of the phoresis had the potential to play a role in the diversification of fea- PAML package4.9 (Yang 2007). The root of the tree was set to a ther lice following the origin of avian-specialized hippoboscid flies maximum age of 80 Mya based on the estimated split of Drosophila (52 Mya). from other Diptera (Misof et al. 2014). This root age was used to Feather louse phoresis on hippoboscid flies is thought to con- estimate the substitution rate across the topology. The split between tribute to known patterns of cophylogenetic incongruence be- and was calibrated to a minimum tween parasite and host tree (Johnson, Adams, et al. 2002, Johnson, age of 42 Mya and the split between Hippoboscoidea and outgroup Weckstein, et al. 2002, Weckstein 2004, Bush et al. 2016). However, Diptera was set to a minimum age of 33 Mya. These two internal certain members of parasitic feather lice are more prone to perform minimum age calibrations were the same used in a larger dating phoresis (Sweet et al. 2018). For example, it has been shown that analysis of Diptera and are considered reliable (Wiegmann et al. feather lice which share a common host and occupy different niches Copyedited by: OUP

Insect Systematics and Diversity, 2019, Vol. 3, No. 4 3

Lipoptena cervi 95% 13-32 Lipopteninae 22 ovinusus 100% 19-328 8 mazamae 100% 7-2113 61% 2399-50 Lipoptena depressa Hippoboscinae equina 100% 99% 14-3424 33-5443 Hippobosca rufipes Olfersini Ortholfersia minutaa 90% 23-434 5 canariensinsis

Crataerina pallida 49% Hippoboscidae 4-127 99% 40-652 3 42% Crataerina hirundinis 5-138 97% fringillinlina Downloaded from https://academic.oup.com/isd/article/3/4/1/5525310 by guest on 24 September 2021 6-159 Ornithomya biloba 99% 9-2014 Ornithomya anchineura 100% Ornithomyini 2-59 100% 95% Ornithomya chloropus 15-3724 6-1610

89% Ornithomya avivulariaia 50-7362 sp.

Basilia boardmani 98% 10-218 7 100% Penicillidia fulvida 18-3827 52% Dipseliopoda setosa Nycteribiidae + 33-5745 Streblidae Brachytarsina speiseri 97% 40-652 3 Paratrichobius longicrurus 95% 10-2918 98% 55-77 67 100% Megistopoda aranea 16-326 7 joblingi

Glossina austeni 93% 5-159 Glossina pallidipes 99% 8-2013 99% 4-13 100% 7 14-321 0 Glossina swynnertoni Glossinidae Glossina palpalis 60-8373 100% 100% 23-535 0 4-169 Glossina fuscipes

Glossina brevipalpis

Cordilura ciliata 98% 34-542 0 69% Hydrophoria lancifer 41-6251 78 30% Lucilia sericata 48-7059 Muscina stabulans 56% 52% 27-60 52-7564 44 Stomoxys calcitrans

Fannia canicularis

Drosophila melanogaster 80 70 60 50 40 30 20 10

8 Mya

Fig. 1. Result of the MCMCTree dating analysis of the published Hippoboscoidea NCBI popset of four genes (CO1, CAD, 16s, 28s; Petersen et al. 2007). Bootstrap support is depicted to the left of nodes. The scale bar depicts divergence estimates in millions of years (Mya) and 95% highest probability distribution (HPD) are to the right of nodes. Red branches represent avian-feeding Hippoboscidae lineages. Feather louse images above scientific names indicate the or species below has records of louse phoresis (Ornithoctona has records of louse phoresis for three species, but the specimen analyzed was not identified to species level; a single record of louse phoresis exists for Crataerina, but is believed to be inaccurate because members of the genus are stenopterous; Corbet 1956, Keirans 1975). Illustrations of to the right of scientific names show host associations of Hippoboscoidea species with true ectoparasitism (Maa 1969).

convergently evolve to a slender wing louse form or larger body form because the slender wing louse morphology more readily form (Johnson et al. 2012). The slender wing form has been suggested facilitates attachment to hippoboscid flies(Johnson et al. 2012, Sweet to have a higher degree of cophylogenetic incongruence relative to the et al. 2018). Copyedited by: OUP

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