High Genetic Load in an Old Isolated Butterfly Population
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High genetic load in an old isolated butterfly population Anniina L. K. Mattila1, Anne Duplouy, Malla Kirjokangas, Rainer Lehtonen, Pasi Rastas, and Ilkka Hanski1 Metapopulation Research Group, Department of Biosciences, University of Helsinki, FI-00014 Helsinki, Finland Edited by Wyatt W. Anderson, University of Georgia, Athens, GA, and approved July 2, 2012 (received for review April 11, 2012) We investigated inbreeding depression and genetic load in a small reversible way. Theoretical models have been constructed to ana- (Ne ∼ 100) population of the Glanville fritillary butterfly(Melitaea lyze the factors influencing the likelihood of mutational meltdown. cinxia), which has been completely isolated on a small island These models have addressed the effects of effective population [Pikku Tytärsaari (PT)] in the Baltic Sea for at least 75 y. As a refer- size (5) and the rate of appearance of new deleterious mutations ence, we studied conspecific populations from the well-studied and their effects (5), as well as compensatory beneficial mutations metapopulation in the Åland Islands (ÅL), 400 km away. A large (20) and epistatic interactions (21). What is in short supply are population in Saaremaa, Estonia, was used as a reference for es- empirical studies of genetic load and its consequences in natural N timating genetic diversity and e. We investigated 58 traits related populations. Previous studies have rarely documented the history to behavior, development, morphology, reproductive perfor- of isolation and past population sizes. In the absence of this in- mance, and metabolism. The PT population exhibited high genetic formation, researchers have merely assumed that small current load (L=1 − WPT/WÅL) in a range of fitness-related traits including L= fl L population size combined with reduced genetic variation is indic- adult weight ( 0.12), ight metabolic rate ( = 0.53), egg viability ative of long-term isolation and that such populations potentially (L = 0.37), and lifetime production of eggs in an outdoor popula- suffer from the accumulation of deleterious mutations (22). In the tion cage (L = 0.70). These results imply extensive fixation of case of naturally isolated insect populations, the focus of research deleterious recessive mutations, supported by greatly reduced di- has been on reduced genetic diversity (23–27). Strong support for versity in microsatellite markers and immediate recovery (hetero- fi sis) of egg viability and flight metabolic rate in crosses with other genetic load due to drift is provided by demonstration of tness populations. There was no significant inbreeding depression in recovery (heterosis) in crosses between isolated populations (28, fi most traits due to one generation of full-sib mating. Resting met- 29). Studies of natural populations have demonstrated tness re- abolic rate was significantly elevated in PT males, which may be covery due to a small number of unrelated immigrants entering an – related to their short lifespan (L=0.25). The demographic history isolated population (14, 30 32) and leading to genetic rescue (33, and the effective size of the PT population place it in the part of 34), regardless of whether reduced fitness was due to inbreeding the parameter space in which models predict mutation accumula- depression (segregation load) or drift (fixation load) (35, 36). tion. This population exemplifies the increasingly common situa- Here, we report on inbreeding depression, genetic load (fit- tion in fragmented landscapes, in which small and completely ness), and local adaptation in a population of the Glanville frit- isolated populations are vulnerable to extinction due to high ge- illary butterfly(Melitaea cinxia) on the small island of Pikku netic load. Tytärsaari (PT) in the northern Baltic Sea. This small population has been completely isolated for at least 75 y. As a reference, we fixation load | segregation load | hybrid vigor | persisting population | use the large conspecific metapopulation in the Åland Islands inbreeding avoidance (ÅL), located 400 km away, which has been intensively studied for the past 20 y (37, 38). The amount of neutral genetic variation lost ampant loss and fragmentation of natural habitats is a prime by the small isolated population is consistent with model pre- Rcause of population and species extinctions. At their final dictions, given its demographic history. We found no convincing stage, extinctions are typically ascribed to ecological processes evidence for local adaptation and only limited inbreeding de- (1), especially to demographic and environmental stochasticities, pression due to one generation of full-sib mating, supporting which increase the risk of extinction for remaining small pop- a high degree of relatedness between individuals and purging of ulations (2–4). However, in the absence of gene flow, the viability strongly deleterious alleles. In contrast, the isolated PT population of isolated remnant populations may be compromised also by exhibits large fitness reduction in comparison with the reference genetic processes, such as inbreeding depression due to segre- population in a range of traits including body size, flight metabolic gation of deleterious recessive mutations and overdominant rate, egg viability, adult longevity, and lifetime production of eggs alleles and mutational meltdown due to fixation of old and new and larvae. Finally, we observed complete fitness recovery (het- deleterious mutations of smaller effect by random genetic drift erosis) in crosses between PT and other regional populations, (5–7). On the other hand, increased homozygosity due to in- implying high genetic load in this isolated population, which may breeding and drift may expose strongly deleterious recessive be undergoing a genetic meltdown to extinction. mutations to selection (8), thereby increasing mean fitness (9, 10), and local adaptation may further enhance fitness in the fl – absence of disruptive gene ow (11 13). Complete isolation and Author contributions: A.L.M. and I.H. designed research; A.L.M., A.D., M.K., and R.L. reduction in population size, which are increasingly common performed research; P.R. contributed new reagents/analytic tools; A.L.M., A.D., M.K., predicaments for populations in human-dominated landscapes R.L., and P.R. analyzed data; and A.L.M., A.D., M.K., R.L., P.R., and I.H. wrote the paper. (14–16), can thus have contrasting effects on population viability. The authors declare no conflict of interest. There are scores of studies focusing on the effects of drift or This article is a PNAS Direct Submission. inbreeding or local adaptation (7, 17, 18), but their joint effects Freely available online through the PNAS open access option. remain little studied and therefore poorly understood (19). 1To whom correspondence may be addressed. E-mail: anniina.mattila@helsinki.fi or ilkka. Increasing frequency and fixation of deleterious recessive mu- hanski@helsinki.fi. tations in isolated populations via inbreeding and drift are a par- See Author Summary on page 14744 (volume 109, number 37). ticularly serious concern for conservation as they may erode This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. population viability gradually, in an initially imperceptible but ir- 1073/pnas.1205789109/-/DCSupplemental. E2496–E2505 | PNAS | Published online August 20, 2012 www.pnas.org/cgi/doi/10.1073/pnas.1205789109 Downloaded by guest on September 29, 2021 PNAS PLUS Results 1+1 founders Population Origin and Genetic Diversity. The Glanville fritillary 0.8 2+2 founders fi 3+3 founders was rst recorded on the small uninhabited island of PT in the 4+4 founders middle of the Gulf of Finland in 1936. The island has a single 5+5 founders meadow of ca. 10 ha with the larval host plant Veronica spicata 0.7 50+50 founders along the shore. The nearest mainland (Estonia) is ca.30km away. The Glanville fritillary was most likely unintentionally in- 0.6 troduced from the Estonian coast by people who used the island as a base for fishing and travel. It is practically certain that there 0.5 has been no further gene flow to the island because it has been Heterozygosity visited very seldom by anyone since World War II (WWII) and the butterfly is a poor disperser (39). Exhaustive surveys of the 0.4 entire habitat area on the island revealed 111 and 198 larval family groups (full siblings) in 2009 and 2011, respectively. Using the formula in Hartl and Clark 2007 (40) and assuming that the 0.3 expected heterozygosities in the initial and current populations 0 20 40 60 80 100 120 are 0.73 and 0.43, respectively (Table 1) and that the age of the Time since colonization population is 100 y (=100 generations), we obtain Ne = 95, Fig. 1. Model-predicted reduction in expected heterozygosity in the PT which is consistent with the above-cited numbers of larval family population with time since the colonization. The results are shown for six groups (some females produce two or even more larval groups different propagule sizes, from a single mated female to 50 females mated that survive until the autumn) (41). with 50 males. Bars giving 1 SD are shown for the propagule size 3+3 and are Data for seven microsatellites indicate closer similarity of the very similar to all other propagule sizes. The propagule is assumed to have PT population to the Estonian population from Saaremaa (SA) the genetic parameters of the Estonian population on the island of Saar- than to the Finnish population from the ÅL (Table 1). The PT emaa (Table 1). The horizontal line gives the expected heterozygosity in the population shares seven alleles in the seven microsatellites with PT population. only the Estonian population, but only one allele with only the < ÅL population (P 0.05). The pairwise Fst values between PT quenced the mitochondrial DNA gene COI, which had only one and Estonia and between PT and ÅL are 0.28 and 0.41, re- haplotype in PT, but this is not informative because the same F spectively, whereas st between Estonia and ÅL is 0.22 (all values haplotype is common in both SA and ÅL, which had five and fi P < statistically signi cant, 0.05).