First genealogy for a wild marine fish population reveals multigenerational philopatry

Abstract

Natal philopatry, the return of individuals to their natal area for reproduction, has advantages and disadvantages for animal populations. Natal philopatry may generate local genetic adaptation, but it may also increase the probability of inbreeding that can compromise persistence. Although natal philopatry is well documented in anadromous fishes, marine fish may also return to their birth site to spawn. How philopatry shapes wild fish populations is, however, unclear because it requires constructing multigenerational pedigrees that are currently lacking for marine fishes. Here we present the first multigenerational pedigree for a marine fish population by repeatedly genotyping all individuals in a population of the orange clownfish (Amphiprion percula) at Kimbe Island (Papua New Guinea) during a 10-y period. Based on 2927 individuals, our pedigree analysis revealed that longitudinal philopatry was recurrent over five generations. Progeny tended to settle close to their parents, with related individuals often sharing the same colony. However, successful inbreeding was rare, and genetic diversity remained high, suggesting occasional inbreeding does not impair local population persistence. Local reproductive success was dependent on the habitat larvae settled into, rather than the habitat they came from. Our study suggests that longitudinal philopatry can influence both population replenishment and local adaptation of marine fishes. Resolving multigenerational pedigrees during a relatively short period, as we present here, provides a framework for assessing the ability of marine populations to persist and adapt to accelerating climate change.Amphiprion percula | self-recruitment | multigenerational pedigree | inbreeding | parental effects

Kin recognition in embryonic damselfishes

“…polyacanthus are both demersal spawners which lay their eggs in caves, and kin recognition is potentially relevant to both species. For those species with a pelagic larval phase, studies have found a high proportion of larvae returning (∼50%), not only to their natal reef, but within metres of their parents at settlement (Jones , Salles et al ).…”

Finding Nemo’s Genes: A chromosome‐scale reference assembly of the genome of the orange clownfishAmphiprion percula

“…The orange clownfish is used as a model species to study patterns and processes of social organization (Buston & Wong, 2014;Buston, Bogdanowicz, Wong, & Harrison, 2007;Wong, Uppaluri, Medina, Seymour, & Buston, 2016), sex change (Buston, 2003), mutualism (Schmiege, D'Aloia, & Buston, 2017), habitat selection (Dixson et al, 2008;Elliott & Mariscal, 2001;Scott & Dixson, 2016), lifespan (Buston & García, 2007) and predator-prey interactions (Dixson, 2012;Manassa, Dixson, McCormick, & Chivers, 2013). It has been central to ground-breaking research into the scale of larval dispersal and population connectivity in marine fishes (Almany et al, 2017;Pinsky et al, 2017;Planes, Jones, & Thorrold, 2009;Salles et al, 2016) and how this influences the efficacy of marine protected areas (Berumen et al, 2012;Planes et al, 2009). It is also used to study the ecological effects of environmental disturbances in marine ecosystems (Hess, Wenger, Ainsworth, & Rummer, 2015;Wenger et al, 2014), including climate change (McLeod et al, 2013;Saenz-Agudelo, Jones, Thorrold, & Planes, 2011) and ocean acidification (Dixson, Munday, & Jones, 2010;Jarrold, Humphrey, McCormick, & Munday, 2017;Munday et al, 2009;Simpson et al, 2011).…”

The formation of marine kin structure: effects of dispersal, larval cohesion, and variable reproductive success

“…Despite the potential for kin disruption, genetic studies have shown that, across major taxonomic groups, pairs of putative siblings, and even family groups, are sometimes found within the same microhabitat or sampling location after settlement (Iacchei et al 2013, Salles et al 2016, Selwyn et al 2016, Riquet et al 2017). These findings challenge conventional views of kinship in the sea and raise questions about how kin associations persist despite the potential for dispersal to disrupt them.…”

“…These patterns all support the notion that long-distance dispersal and gene flow can be common in the marine environment. Nevertheless, genetic parentage studies have revealed limited dispersal in some species (D'Aloia et al 2015, Salles et al 2016; therefore, it remains a plausible explanation for marine kin structure.…”