Elsevier

Biological Conservation

Volume 249, September 2020, 108710
Biological Conservation

Long term effects of outbreeding: experimental founding of island population eliminates malformations and improves hatching success in sand lizards

https://doi.org/10.1016/j.biocon.2020.108710Get rights and content

Highlights

  • Fragmented populations are often inbred with low genetic diversity.

  • Outbreeding with other populations can rescue genetic diversity.

  • Sand lizard populations of Southern Sweden are threatened by inbreeding.

  • Outbreeding improved offspring viability of sand lizards for six generations.

Abstract

Loss of genetic variation is an increasing problem in many natural populations as a result of population fragmentation, inbreeding, and genetic drift, which may lead to inbreeding depression and subsequent “extinction vortices”. In such cases, outbreeding offers a potential population saviour from extinction. Here we compare offspring viability between an experimentally founded outbred island population of sand lizards Lacerta agilis, and an inbred mainland source population on the Swedish West coast. We have studied the mainland population for over a decade during which >4000 offspring from >500 parents were monitored. We conducted an outbreeding experiment in which lizards from the mainland population with relatively low genetic variation were crossbred with lizards from distant populations that lack gene flow. The resulting 454 offspring were introduced to an otherwise uninhabited island with ideal sand lizard habitat. A survey of the island two decades later showed that offspring produced by females from the experimentally founded population had 13% higher hatching success (99.3% versus 86.4%) and elimination of the malformations occurring in 21% of clutches in the mainland source population. These results co-occur with higher genetic diversity. We conclude that outbreeding improved offspring viability in our island population ca 5–6 generations after the founding event, that is, with sustained viability effects at a time when heterotic effects are expected to have subsided.

Introduction

The number of species and populations suffering from loss of genetic variation has increased over recent decades for a variety of reasons including overharvest, loss of suitable habitat, and population fragmentation (Ehrlich, 1988; Keller and Waller, 2002). Both inbreeding and genetic drift can exacerbate losses to genetic diversity of these fragmented populations (Hartl et al., 1997). In a majority of small and isolated populations studied to date, these reductions in genetic diversity and inbreeding have significant negative effects on organismal fitness, such as decreased survival in female bighorn lamb (Rioux-Paquette et al., 2011), decreased hatching success in birds (Blomqvist et al., 2010; Bouzat et al., 1998), and increased risk of malformations and decreased viability in adder snake offspring (Madsen et al., 1996).

Inbreeding depression is the accumulation of detrimental effects on fitness traits including survival and offspring fertility resulting from matings between close relatives and an increase in homozygosity leading to adverse gene combinations (Charlesworth and Willis, 2009). Inbreeding depression can accelerate fitness decline with populations forced into an “extinction vortex” when negative genetic, environmental, and demographic factors act together and compromise a population's probability of future survival (Fagan and Holmes, 2006; Nabutanyi and Wittmann, 2020). In such cases, conservation through protection of the population or its habitat is not sufficient to maintain population viability but may need to be complemented with introgression of beneficial genetic variants through low level immigration (to avoid disruption of locally adapted genotypes, i.e. ‘swamping’ Hedrick and Garcia-Dorado, 2016; Whiteley et al., 2015). While deliberate outbreeding may involve risk due to outbreeding depression (Hedrick and Garcia-Dorado, 2016; Whiteley et al., 2015), this risk is thought to be low for populations occupying similar environments who only recently diverged (<500 years, Frankham et al., 2011), and the benefits of genetic rescue on fitness are consistently high (Frankham, 2015). However, the number of outbreeding events required and the duration of outbreeding effects on population fitness may vary based on species life-history, necessitating long term studies on outbreeding and genetic rescue (Frankham, 2016; Hedrick and Garcia-Dorado, 2016; Whiteley et al., 2015). Here we present results from an outbreeding study in a closed (island) population of sand lizards (Lacerta agilis) 20 years subsequent to its experimental founding (ca. 5–6 generations based on a conservative 4–5 year delay between birth of an individual and its offspring).

Our aim with the current analysis is to assess the long-term effects of outbreeding on offspring viability in the sand lizard. To address this, we analysed data collected from two populations of sand lizards. First, we utilize a long-term data set collected from a mainland population with low level genetic variation (hereafter ‘mainland’; Gullberg et al., 1998; Gullberg et al., 1999) and negative effects on offspring viability at mating between siblings (Bererhi et al., 2019; Olsson et al., 1996). In a laboratory breeding experiment, adult males and females from this focal mainland population were mated with males and females captured in Southern Swedish populations that lacked genetic exchange (Olsson et al., 2018). The ostensibly outbred offspring from these matings (n = 454) were released to establish our second focal population on a small island off the Swedish west coast (hereafter ‘island’) 15 km to the north of our mainland population. This island lacked resident sand lizards but had suitable habitat structure, composition of vegetation, and availability of insect prey.

We asked the following questions with respect to differences between our outbred island and inbred mainland populations: Do descendants from outbred offspring (i) suffer less from infertility, have (ii) higher hatching success, and (iii) lower risk of having malformed young? Some viability effects, such as hatching success and risk of malformations, are responsive to non-genetic factors such as female calcium deficiency which can yield offspring with underdeveloped egg teeth less capable of hatching (Frye, 1991). Heterogametic females (ZW) could also be more affected by outbreeding than homogametic (ZZ) males (when deleterious recessives have 100% expression). We therefore also ask whether (iv) island and mainland females differ in offspring sex ratios and female reproductive investments, potential sources of bias in our measurement of offspring viability.

Section snippets

Study species

The sand lizard is a small ground-dwelling lizard up to 200 mm head to tail tip and weighing up to 20 g. The sand lizard is a red-listed species in Sweden and therefore of high conservation interest (Niesel, 2007). It has a large distribution from central Asia in the East to United Kingdom in the West, and from the Mediterranean in the South to Sweden in the North (IUCN, 2010). Populations of the Swedish sand lizard are highly fragmented with little or no inter-population gene flow (Olsson et

Results

From 1998 to 2008, 367 females from the mainland population were brought in to the laboratory where they laid a total of 4277 eggs. In 2017, 24 females from the island were brought in to the laboratory where they laid a total of 166 eggs.

Discussion

Sand lizards on our mainland source population have low levels of genetic variation (Bererhi et al., 2019; Olsson et al., 1996) associated with elevated risks of offspring malformation, the combination of which is indicative of inbreeding depression. To counter that effect, we outbred adults from this population with those from populations well outside normal migration distance (Olsson et al., 1996). Short term improvements in offspring viability could easily have been explained by heterosis,

Data availability

Data will be made available at dryad digital repository.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We thank the Swedish Science Council (VR) and the Australian Research Council for financial support (to MO). Genome sequencing was performed by the SNP&SEQ Technology Platform in Uppsala, which is part of Science for Life Laboratory at Uppsala University and is supported as a national infrastructure by the Swedish Research Council (VR-RFI) and the Knut and Alice Wallenberg Foundation. For computational resources, we thank the Uppsala Multidisciplinary Center for Advanced Computational Science

Author statement

Willow Lindsay: Conceptualization, Writing – Original Draft, Review and Editing, Investigation, Supervision Thomas Madsen: Investigation, Writing – Review and Editing Erik Wapstra: Conceptualization, Investigation, Writing –Review and Editing Mette Lillie: Methodology, Investigation, Formal Analysis, Writing – Review and Editing Lisa Loeb: Investigation, Writing – Review and Editing Beata Ujvari: Investigation, Writing – Review and Editing Mats Olsson: Conceptualization, Writing – Original

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