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Conservation: Bye-Bye to the Hihi?

2019; Elsevier BV; Volume: 29; Issue: 6 Linguagem: Inglês

10.1016/j.cub.2019.02.013

1879-0445

Nancy Chen,

Evolution and Genetic Dynamics

Theoretically, small populations should be less capable of adapting to environmental change, yet empirical evidence is mixed. A new study on a rare New Zealand bird, the Hihi, uses genomics and long-term demographic data to reveal low adaptive potential. Theoretically, small populations should be less capable of adapting to environmental change, yet empirical evidence is mixed. A new study on a rare New Zealand bird, the Hihi, uses genomics and long-term demographic data to reveal low adaptive potential. Populations of many animal species are declining at an unprecedented rate across the world [1Ceballos G. Ehrlich P.R. Dirzo R. Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines.Proc. Natl. Acad. Sci. USA. 2017; 114: E6089-E6096Crossref PubMed Scopus (1183) Google Scholar]. To prevent extinction, a thorough understanding of the factors affecting the persistence of small populations is paramount. Small populations are more likely to go extinct due to stochastic effects [2Lande R. Genetics and demography in biological conservation.Science. 1988; 241: 1455-1460Crossref PubMed Scopus (1652) Google Scholar] and may face additional threats due to inbreeding depression, the loss of genetic diversity and the accumulation of deleterious mutations [3Frankham R. Genetics and extinction.Biol. Cons. 2005; 126: 131-140Crossref Scopus (1547) Google Scholar, 4Frankham R. Ballou J. Briscoe D. Introduction to Conservation Genetics. Cambridge University Press, Cambridge, UK2003Google Scholar]. Given the rapid rate of global environmental change, a particular concern is that small populations are predicted to have lower adaptive potential, that is, a reduced capacity to change genetically in response to environmental changes [5Willi Y. Van Buskirk J. Hoffmann A.A. Limits to the adaptive potential of small populations.Annu. Rev. Ecol. Evol. S. 2006; 37: 433-458Crossref Scopus (599) Google Scholar]. The adaptive potential of a population is ultimately determined by the amount of heritable genetic variation for fitness available in the population [6Falconer D.S. Mackay T.F.C. Introduction to Quantitative Genetics.4th Edition. Longman, Harlow, 1996Google Scholar]. Despite the importance of adaptive potential in predicting population persistence, measuring adaptive potential in natural populations is exceedingly difficult, and rigorous studies of adaptive potential in threatened populations remain rare [7Hoffmann A.A. Sgrò C.M. Kristensen T.N. Revisiting adaptive potential, population size, and conservation.Trends Ecol. Evol. 2017; 32: 506-517Abstract Full Text Full Text PDF PubMed Scopus (122) Google Scholar]. A recent paper in Current Biology by Pierre de Villemereuil, Anna W. Santure, and colleagues [8de Villemereuil P. Rutschmann A. Lee K.D. Ewen J.G. Brekke P. Santure A.W. Little adaptive potential of a threatened passerine.Curr. Biol. 2019; 29: 889-894Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar] uses multiple methods to assess the adaptive potential of an endemic New Zealand bird, the hihi (Notiomystis cincta). The hihi, or stitchbird, is a small songbird that is one of New Zealand’s rarest birds and the sole member of the endemic family Notiomystidae [9Driskell A. Christidis L. Gill B.J. Boles W.E. Barker F.K. Longmore N.W. A new endemic family of New Zealand passerine birds: adding heat to a biodiversity hotspot.Aust. J. Zool. 2007; 55: 73-78Crossref Scopus (50) Google Scholar]. Males have white ear tufts and a black head ringed by bright yellow shoulders, while females are a drab olive (Figure 1). These curious birds flit through the forest canopy, tails cocked, often emitting the distinct ‘stitch' call that gave the stitchbird its English name [10Buller W.L. Fam. TIMELIPHGIDÆ — Pogonornis Cincta. — (Stitch-Bird).in: A History of the Birds of New Zealand. Second Edition. Walter Buller, London1888Crossref Google Scholar]. The hihi feeds on nectar, fruits and invertebrates, but their food choice is largely determined by local competitors — the larger, more dominant tui and bellbirds get the first pick in foraging sites [11Taylor S. Castro I.C. Griffiths R. Hihi/stitchbird (Notiomystis Cincta) Recovery Plan, 2004-09. Department of Conservation, 2005Google Scholar]. Hihi have unusual reproductive behavior: they have a highly variable and promiscuous mating system and are the only known bird that mates face to face [12Castro I. Minot E.O. Fordham R.A. Birkhead T.R. Polygynandry, face-to-face copulation and sperm competition in the Hihi Notiomystis cincta (Aves: Meliphagidae).IBIS. 1996; 138: 765-771Crossref Scopus (55) Google Scholar]. Its Maori name, hihi, means ‘ray of sunshine'. In Maori folklore, the demigod Maui asked the hihi to fetch him some water after he tamed the sun. When the bird refused, Maui picked him up and threw him into the fire, burning his feathers. The male hihi’s yellow and black plumage now serves as a reminder of the sun and fire, a permanent lesson about disobedience [13Keane, K. ‘Ngā manu – birds', Te Ara - the Encyclopedia of New Zealand.Google Scholar]. The hihi was once commonly found throughout the North Island and several offshore islands of New Zealand. Its numbers declined rapidly after the arrival of European settlers, likely due to the usual factors that impact endemic species: habitat loss and introduced predators — in this case, rats — and perhaps new diseases. By the 1880s, this brightly colored bird had disappeared completely from the mainland, and could only be spotted in the forests of Te Hauturu-o-Toi, Little Barrier Island [11Taylor S. Castro I.C. Griffiths R. Hihi/stitchbird (Notiomystis Cincta) Recovery Plan, 2004-09. Department of Conservation, 2005Google Scholar]. Fortunately for these birds, a massive conservation effort beginning in the 1980s has removed mammalian predators and successfully reintroduced the hihi to six sites throughout its historical range [14Brekke P. Bennett P.M. Santure A.W. Ewen J.G. High genetic diversity in the remnant island population of hihi and the genetic consequences of re-introduction.Mol. Ecol. 2011; 20: 29-45Crossref PubMed Scopus (63) Google Scholar]. One of these sanctuaries is on the island of Tiritiri Matangi. Here, the hihi population has been intensively managed since it was first established in 1995. All individuals are given a unique set of color bands on their legs, permitting individual identification (Figure 1), and the birds are provided supplemental food and nest boxes in which to raise their young. The nest boxes also help researchers and volunteers monitor all nesting attempts in the population, ensuring that all nestlings are systematically measured, sampled, and banded [15Armstrong D.P. Ewen J.G. Consistency, continuity and creativity: long-term studies of population dynamics on Tiritiri Matangi Island.NZ J. Ecol. 2013; 37: 288Google Scholar]. Over the past few decades, the long-term monitoring of the hihi population on Tiritiri Matangi has generated morphometric and fitness measures for hundreds of individuals, overcoming one of the biggest challenges of evolutionary studies in natural populations: the measurement of individual fitness for large numbers of individuals. This valuable dataset allowed de Villemereuil and colleagues [8de Villemereuil P. Rutschmann A. Lee K.D. Ewen J.G. Brekke P. Santure A.W. Little adaptive potential of a threatened passerine.Curr. Biol. 2019; 29: 889-894Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar] to assess the adaptive potential of the hihi in three separate analyses. First, they assembled a draft genome for the species, then used a reduced representation sequencing approach [16Baird N.A. Etter P.D. Atwood T.S. Currey M.C. Shiver A.L. Lewis Z.A. Selker E.U. Cresko W.A. Johnson E.A. Rapid SNP discovery and genetic mapping using sequenced RAD markers.PLoS One. 2008; 3: e3376Crossref PubMed Scopus (2346) Google Scholar] to survey genomic variation in both Te Hauturu-o-Toi, the last remaining natural population, and Tiritiri Matangi, the primary study population. Levels of nucleotide diversity in both populations were extremely small — smaller than any comparable estimates for other songbirds and similar to estimates from other threatened species [8de Villemereuil P. Rutschmann A. Lee K.D. Ewen J.G. Brekke P. Santure A.W. Little adaptive potential of a threatened passerine.Curr. Biol. 2019; 29: 889-894Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar]. While overall levels of molecular genetic diversity can serve as a proxy for adaptive potential, what really matters for a population’s ability to adapt is heritable genetic variation for traits associated with fitness [17Hoffmann A.A. Willi Y. Detecting genetic responses to environmental change.Nat. Rev. Genet. 2008; 9: 421-432Crossref PubMed Scopus (397) Google Scholar]. Inferences based solely on genomic data are therefore limited by how little we know about the genetic basis of adaptation in most natural populations. Alternatively, in systems where it is possible to obtain phenotypic data from individuals of known relatedness, quantitative genetic approaches can provide a more direct assessment of adaptive potential [17Hoffmann A.A. Willi Y. Detecting genetic responses to environmental change.Nat. Rev. Genet. 2008; 9: 421-432Crossref PubMed Scopus (397) Google Scholar]. Adaptive potential is most directly quantified by the additive genetic variance for fitness, or for a phenotypic trait linked to fitness [18Funk W.C. Forester B.R. Converse S.J. Darst C. Morey S. Improving conservation policy with genomics: a guide to integrating adaptive potential into U.S. Endangered Species Act decisions for conservation practitioners and geneticists.Conserv. Genet. 2018; : 1-20https://doi.org/10.1007/S10592-018-1096-1Crossref Google Scholar]. Additive genetic variance is a measure of how much phenotypic variation can be attributed to the inheritance of alleles from parents to offspring, and is sometimes expressed in terms of heritability, the proportion of phenotypic variation due to additive genetic variation. Traditionally, the additive genetic variance for a given quantitative trait is estimated using controlled breeding experiments [6Falconer D.S. Mackay T.F.C. Introduction to Quantitative Genetics.4th Edition. Longman, Harlow, 1996Google Scholar]. Large breeding experiments, of course, are not feasible for most threatened species. In natural populations with pedigree information or substantial genomic data, one can estimate relatedness among phenotyped individuals and then calculate additive genetic variance using mixed models known as animal models [19Kruuk L.E.B. Estimating genetic parameters in natural populations using the ‘animal model’.Philos. Trans. R. Soc. Lond. B Biol. Sci. 2004; 359: 873-890Crossref PubMed Scopus (825) Google Scholar]. To date, few estimates of additive genetic variance for lifetime reproductive success exist, due to the difficulties of collecting data on fitness in natural populations and the paucity of studies that fit statistical models that appropriately deal with the non-Gaussian distribution of fitness [20Hendry A.P. Schoen D.J. Wolak M.E. Reid J.M. The Contemporary Evolution of Fitness.Annu. Rev. Ecol. Evol. Syst. 2018; 49: 457-476Crossref Scopus (62) Google Scholar]. Using the long-term pedigree and phenotypic data, de Villemereuil and colleagues [8de Villemereuil P. Rutschmann A. Lee K.D. Ewen J.G. Brekke P. Santure A.W. Little adaptive potential of a threatened passerine.Curr. Biol. 2019; 29: 889-894Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar] estimated the additive genetic variance and heritability for lifetime reproductive success, a measure of fitness, as well as a number of morphological and life-history traits that were under selection, such as body mass, adult longevity and the number of eggs. All the measured phenotypes had an extremely low additive genetic variance and heritability, lower than most published estimates for those traits in other species [8de Villemereuil P. Rutschmann A. Lee K.D. Ewen J.G. Brekke P. Santure A.W. Little adaptive potential of a threatened passerine.Curr. Biol. 2019; 29: 889-894Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar]. Thus, there are three indications of limited adaptive potential in the hihi: low genome-wide genetic diversity, low additive genetic variance for a suite of traits under selection and low additive genetic variance for a measure of fitness. So do the findings of de Villemereuil and colleagues [8de Villemereuil P. Rutschmann A. Lee K.D. Ewen J.G. Brekke P. Santure A.W. Little adaptive potential of a threatened passerine.Curr. Biol. 2019; 29: 889-894Abstract Full Text Full Text PDF PubMed Scopus (37) Google Scholar] spell doom for the hihi? Not necessarily. Yes, this study quite thoroughly demonstrates a lack of immediate adaptive potential in the Tiritiri Matangi population. This result is not particularly surprising given the rapid decline of the species and the restriction to a single population on Te Hauturu-o-Toi for over a century [14Brekke P. Bennett P.M. Santure A.W. Ewen J.G. High genetic diversity in the remnant island population of hihi and the genetic consequences of re-introduction.Mol. Ecol. 2011; 20: 29-45Crossref PubMed Scopus (63) Google Scholar]. Furthermore, we still don't know much about other factors that may increase extinction risk in this species, such as inbreeding depression and genetic load. On the flip side, the population on Tiritiri Matangi seems demographically healthy — it is so productive that it serves as a source population for translocations to other sites [15Armstrong D.P. Ewen J.G. Consistency, continuity and creativity: long-term studies of population dynamics on Tiritiri Matangi Island.NZ J. Ecol. 2013; 37: 288Google Scholar] — and we know of populations that seem to be stable despite low levels of genetic variation (e.g., the Channel Island Fox and Chillingham cattle) [7Hoffmann A.A. Sgrò C.M. Kristensen T.N. Revisiting adaptive potential, population size, and conservation.Trends Ecol. Evol. 2017; 32: 506-517Abstract Full Text Full Text PDF PubMed Scopus (122) Google Scholar]. Moreover, estimates of additive genetic variance are specific to the population and environmental context in which the phenotype was measured, and can vary as allele frequencies and environmental conditions change [6Falconer D.S. Mackay T.F.C. Introduction to Quantitative Genetics.4th Edition. Longman, Harlow, 1996Google Scholar]. We therefore do not know if all other hihi populations also have low additive genetic variance for fitness — though it seems likely — and we cannot necessarily make predictions about the adaptive potential of populations far in the future. Indeed, predicting the long-term future viability of a population and determining the best management strategy for threatened populations remain complicated, difficult issues. It will be fascinating to see whether, and how, adaptive potential changes as the hihi population grows in size.