10/8/14 Brood Parasitic Estrildid Finch Host Finches Species Pin-tailed whydah Common Waxbill Vidua macroura Estrilda astrild by Justin Schuetz 1 10/8/14 Indigobirds parasitize firefinches (and a few others) Indigobird species… ² …are highly host-specific, most species parasitizing a single estrildid finch host species ² …mimic the nestling mouth colors and patterns of their respective hosts ² …are morphologically distinct (in juvenile mouth markings and adult male morphology) but only slightly differentiated in neutral genetic markers ² …learn and mimic host songs, resulting in assortative mating and providing a mechanism for rapid sympatric diversification by host shift 2 10/8/14 3 10/8/14 V. camerunensis (black-bellied firefinch mimic) V. camerunensis (African firefinch mimic) V. raricola (goldbreast mimic) Chatter Complex non-mimicry Mimicry Balakrishnan & Sorenson 2007 Behav Ecol host nest host nest black-bellied black-bellied firefinch firefinch indigobird mimics black- mate indigobird imprinted on bellied firefinch song choice black-bellied firefinch parasitism of novel or alternate host host choice black-bellied African firefinch firefinch indigobird mimics African firefinch song or indigobird imprinted on African firefinch *Tested in captive birds by Payne et al. 1998, 2000 Anim Behav Figure from Edwards et al. 2005 PNAS 4 10/8/14 But… v don’t the same mechanisms promoting speciation also lead to hybridization? v indigobirds from eggs laid in the nest of an “alternate” host will imprint on the “wrong” host and later hybridize with individuals of the indigobird species associated with that hosta Association of mimicry song and morphology in 494 male indigobirds* N male indigobirds Vidua mimicry song cha. fun. pur. cod. L. senegala 306 0 0 0 L. rubricata 1 63 0 1 L. rhodopareia 2 0 84 0 H. niveoguttatus 0 0 0 37 total mismatches 4/494 = 0.8% *localities in S-C Africa with two or more Vidua species Payne et al. 1992 Proc. PAOC 5 10/8/14 The question: How “good” are indigobird species? v Are indigobirds early in the process of evolving into fully distinct and reproductively isolated species? v Or, are they stuck in a perpetual state of incomplete speciation due to imperfect isolating mechanisms? Higher nucleotide diversity in one species of firefinch than in all 10 species of indigobirds combined 0.1 each point represents one 0.01 locus 0.001 0.0001 Red-billed Firefinches (n=10) 0.00001 0.00001 0.0001 0.001 0.01 0.1 Indigobirds (10 species, n=72) 6 10/8/14 Phylogeny of indigobird mtDNA haplotypes V. codringtoni V. purpurascens V. funerea V. chalybeata V. nigeriae V. maryae V. wilsoni V. raricola V. larvaticola V. camerunensis Network of West African haplotypes: Cameroon & Nigeria ΦST = 0.41 p < 0.00001 microsatellites (11 loci) FST = 0.017 p < 0.0001 Sorenson et al. 2003 Nature 7 10/8/14 Ancestral polymorphism Species 1 Species 2 S1 S2 Time Lineage sorting 2N -4N generations e e Ancestral population Indigobirds: gene flow plus lineage sorting Species 1 Species 2 S1 S2 Time Ancestral population How to separate historical effects from current dynamics?? 8 10/8/14 IM - Isolation with Migration v model of population divergence v Nielsen & Wakeley 2001 Genetics v Hey 2005 PLoS Biology Testing hypotheses… v what is the likelihood L (=probability) of the observed data? L = Pr{D | G,µ}Pr{G |α} ∑ G v L = the sum across all possible genealogies (G) of the probability of the data given the genealogy and a model of the mutation process (µ) times the probability of the genealogy given € a set of parameters (α) that characterize the population process 9 10/8/14 In practice… v for a sample of k alleles, draw random coalescence times according to the exponential distribution v estimate the likelihood (probability) of observing the actual data on that genealogy v change a parameter, generate a new genealogy, calculate likelihood, repeat millions of times Markov Chain Monte Carlo methods 10 10/8/14 IM - Isolation with Migration v model of population divergence v Nielsen & Wakeley 2001 Genetics v Hey 2005 PLoS Biology Phylogeny of indigobird mtDNA haplotypes V. codringtoni V. purpurascens V. funerea V. chalybeata V. nigeriae V. maryae V. wilsoni V. raricola V. larvaticola V. camerunensis 11 10/8/14 V. chalybeata (n = 11) V. camerunensis (n = 11) V. larvaticola (n = 8) V. chalybeata (n = 4) V. camerunensis (n = 3) V. wilsoni (n = 3) V. raricola (n = 3) V. maryae (n = 3) V. nigeriae (n = 3) V. larvaticola (n = 3) • 14 nuclear sequence loci (~300 bp each) • 3 HapSTR loci (~250 bp + STR) V. chalybeata (n = 5) V. codringtoni (n = 5) V. funerea (n = 5) V. purpurascens (n = 5) haplotype diversity at 5 nuclear loci in 10 species 12 10/8/14 IM analyses using 9 nuclear sequence loci 0.1 average = 64K years Posterior Probability 0 0 200 400 600 800 1000 Thousands of Years Before Present IM analyses using 9 nuclear sequence loci 0.02 average = 1.3% 0.01 Posterior Probability 0 0 0.1 0.2 0.3 0.4 0.5 "Splitting Parameter" (s) 13 10/8/14 IM analyses using 9 nuclear sequence loci 0.002 0.001 0.001 Posterior Probability Posterior Probability 0 0 0 2 4 6 8 10 0 2 4 6 8 10 Migration to West (m2) Migration to South (m1) Conclusions 1 v Indigobirds colonized southern Africa ~105 years ago and subsequently evolved into four distinct species! v Coalescent analyses indicate a small founding population for southern Africa followed by substantial expansion 14 10/8/14 Network of indigobird mtDNA haplotypes: Malawi, Zambia, and Zimbabwe Sorenson et al. 2003 Nature Conclusions 2 v Relatively greater genetic differentiation among indigobird species in the ancestral region of West Africa suggests that indigobird species may be slowly diverging from each other and evolving into truly independent evolutionary lineages 15 .