Mixed Mating in a Multi-Origin Population Suggests High Potential for Genetic Rescue in North Island Brown Kiwi, Apteryx mantelli

Abstract

Reinforcement translocations are increasingly utilised in conservation with the goal of achieving genetic rescue. However, concerns regarding undesirable results, such as genetic homogenisation or replacement, are widespread. One factor influencing translocation outcomes is the rate at which the resident and the introduced individuals interbreed. Consequently, post-release mate choice is a key behaviour to consider in conservation planning. Here we studied mating, and its consequences for genomic admixture, in the North Island brown kiwi Apteryx mantelli population on Ponui Island which was founded by two translocation events over 50 years ago. The two source populations used are now recognised as belonging to two separate management units between which birds differ in size and are genetically differentiated. We examined the correlation between male and female morphometrics for 17 known pairs and quantified the relatedness of 20 pairs from this admixed population. In addition, we compared the genetic similarity and makeup of 106 Ponui Island birds, including 23 known pairs, to birds representing the source populations for the original translocations. We found no evidence for size-assortative mating. On the contrary, genomic SNP data suggested that kiwi of one feather did not flock together, meaning that mate choice resulted in pairing between individuals that were less related than expected by random chance. Furthermore, the birds in the current Ponui Island population were found to fall along a gradient of genomic composition consistent with non-clustered representation of the two parental genomes. These findings indicate potential for successful genetic rescue in future Apteryx reinforcement translocations, a potential that is currently under utilised due to restrictive translocation policies. In light of our findings, we suggest that reconsideration of these policies could render great benefits for the future diversity of this iconic genus in New Zealand.

Predicting breeding systems to guide conservation strategies: A kiwi example

“…Kiwi have poor eyesight but a very well‐developed sense of smell (Corfield et al, 2014) and a huge uropygial gland (Reynolds et al, 2017). These physiological features suggest that chemical identification and evaluation of, for instance, mates might occur (Castro et al, 2010; Cunningham et al, 2009) and that mate‐choice, indeed, seems to be active and disassortative in NI brown kiwi (Undin, Lockhart, Hills, Armstrong, & Castro, 2021c). Kiwi are extraordinarily long‐lived, with individuals known to have reached over 40 years and the maximum lifespan suggested to be up to 80 or 100 years (Barlow, 2011; Robertson & Colbourne, 2004; Weiser et al, 2013).…”

“…(3) Directly linked to the latter, the prevalence of polygamy may compensate for a small founder population size. Among other things, this compensation means that the current strict cut off at a founder size of 40 individuals to consider a historic translocation successful (Germano et al, 2018; Jahn et al, 2022) may need to be re‐evaluated (Undin, Hills, Lockhart, & Castro, 2021a; Undin, Lockhart, Hills, Armstrong, & Castro, 2021c; Undin, Lockhart, Hills, & Castro, 2021b). (4) The higher the prevalence of polygamy, the harder it will be to assume relatedness between individuals based solely on the identity of the incubating male (cf.…”

“…We suggest that the lack of distinguishing morphological features, the long lifespan, and the highly developed olfaction, in combination with the three reasons listed above, make NI brown kiwi an interesting study system for mate‐choice as well. Lastly, we suggest that there could be substantial benefits of utilizing genomics (i.e., genome wide genetics) in the studies of NI brown kiwi breeding (Galla et al, 2020; Kardos et al, 2016; Oyler‐McCance et al, 2016; Putman & Carbone, 2014; Semenov et al, 2017; Thavornkanlapachai et al, 2019; Undin, Lockhart, Hills, Armstrong, & Castro, 2021c). For instance, individual and population‐level genomic make‐up can be used to analyze effective population size, admixture, breeding behavior, and mate‐choice over time, as well as the effectiveness of conservation interventions (Galla et al, 2020; Semenov et al, 2017; Thavornkanlapachai et al, 2019; Undin, Lockhart, Hills, Armstrong, & Castro, 2021c).…”

“…Lastly, we suggest that there could be substantial benefits of utilizing genomics (i.e., genome wide genetics) in the studies of NI brown kiwi breeding (Galla et al, 2020; Kardos et al, 2016; Oyler‐McCance et al, 2016; Putman & Carbone, 2014; Semenov et al, 2017; Thavornkanlapachai et al, 2019; Undin, Lockhart, Hills, Armstrong, & Castro, 2021c). For instance, individual and population‐level genomic make‐up can be used to analyze effective population size, admixture, breeding behavior, and mate‐choice over time, as well as the effectiveness of conservation interventions (Galla et al, 2020; Semenov et al, 2017; Thavornkanlapachai et al, 2019; Undin, Lockhart, Hills, Armstrong, & Castro, 2021c). Another example is that genomic traces of fluctuations in population size and diversity can be related to breeding system and reproductive output to increase our understanding of inbreeding depression (Kardos et al, 2016).…”

“…Mate‐choice is closely linked to the breeding system, directly impacts translocation outcomes (Undin, Lockhart, Hills, Armstrong, & Castro, 2021c), and has likely been affected by anthropogenic impact even more than breeding systems. Thus, studies of mate‐choice in relation to lowered population density, habitat modification, and reduced connectivity, are also important for improving conservation management.…”