Inbreeding and Families: How To Save Australia’s Orange-Bellied Parrot

When just a few family lineages dominate the overall genetic diversity in small, endangered populations, these populations become highly inbred, making them vulnerable to catastrophes like disease outbreaks

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When a family lineage produces no surviving descendants, its genetic diversity is lost, and when the population is very small, this loss of family lineages substantially decreases the population’s genetic diversity. When some families produce many offspring that live to reproduce whilst others produce none at all, this is known as reproductive skew, and it is a serious conservation problem for rare species in captive breeding and reintroduction programs, such as the black rhinoceros, Diceros bicornis, and the Floreana Island Galapagos giant tortoise, Chelonoidis niger (ref & ref). Reproductive skew intensifies inbreeding (ref) in an already small population, thereby decreasing the likelihood that the entire population can survive long-term (ref).

In some small wildlife populations, such as the cheetah, Acinonyx jubatus, most individuals alive today may be descendants of only a few individuals (ref) — or in extreme cases, such as that of Aotearoa New Zealand’s Chatham Island black robin, Petroica traversi, just one pair (ref). Thus, even when the total population may be large, all its individuals could be close relatives so the overall genetic diversity could be very low (ref). For this reason, it’s important to monitor lineage loss in conserved wildlife populations, despite the fact that collecting the required genetic data to detect and accurately measure it can be quite challenging. Due to the difficulties involved, this reproductive skew is poorly studied, although we do know its impacts are not good.

Australia’s critically endangered orange-bellied parrots, Neophema chrysogaster, are a tiny and decreasing population of migratory parrots. Although these small parrots can live up to 11 years, few of them actually live long enough to breed more than once in their lives and further, juveniles have an extremely high mortality rate (ref). But are these juvenile deaths random or are they non-random? For example, because siblings have a similar start in life, maybe the odds are if one chick dies before reaching reproductive age, all of its siblings are much more likely to die young too?

Conservation biologist, Dejan Stojanovic, a postdoctoral fellow at the Australian National University and lead postdoc with the Difficult Birds Research Group, wondered what happens to small conserved populations when high juvenile mortality is non-random amongst siblings. He and his collaborators realized that orange-bellied parrots could help provide some answers. They analyzed 22 years (1995 to 2017) of field data collected by staff and volunteers from the wild orange-bellied parrot population, to:

1. quantify how often individuals fail to produce any living descendants due to non-random juvenile mortality of sibling parrots
2. identify living maternal lineages and quantify how many surviving descendants produced by each parrot mother, and
3. evaluate the demographic impacts of non-random juvenile mortality of sibling parrots using population viability analysis (PVA), an important statistical tool for modelling population size, genetic diversity and extinction risk over time

First, Dr Stojanovic and his collaborators documented that non-random juvenile mortality of sibling parrots occurred more frequently than expected by chance. They found that the ratio of observed (black bars, Figure 2) versus expected (grey bars, Figure 2) non-random juvenile sibling mortality was 1.37, which means that, if one chick died in its first year of life, all of its siblings were 1.37 times more likely to die in their first year of life too.

In a large and thriving population, the loss of a family lineage is what the process of natural selection looks like, and thus, it serves to ensure that only the healthiest lineages are passing on their genes to future generations. But because wild orange-bellied parrot females usually have just one opportunity to breed in their lives, a failed breeding attempt is a disaster because that individual produces no living descendants.

“I was shocked that within just three years 9/10 remaining wild family lineages died out, leaving a single mother representing the entire evolutionary history of this species in the wild”, Dr Stojanovic told me in email.

In tiny, inbred populations, loss of a family lineage can be a big problem because family lineages form the genetic substructure of populations. Further, in tiny populations, like orange-bellied parrots, some families may possess important genetic diversity that, if lost, diminishes the overall genetic diversity of the entire species.

This genetic diversity can’t be replaced once it’s lost.

Dr Stojanovic and his collaborators used PVA analyses to determine potential outcomes for two mortality scenarios: random juvenile mortality and non-random juvenile mortality amongst parrot siblings. They created two scenarios, Pair One (upper panel, Figure 3) is the ‘optimistic model’ based on 1995 juvenile mortality rates (49%). It showed that, if conservation efforts are successful and juvenile mortality could be reduced to pre-1995 levels, then the population may possibly survive non-random juvenile mortality amongst parrot siblings despite the resulting decline in genetic diversity (pink line).

On the other hand, Pair Two (lower panel, Figure 3) was based on the current high juvenile mortality rates (80%) documented in orange-bellied parrots. Simulating the current high non-random juvenile mortality amongst parrot siblings resulted in substantially reduced genetic diversity, rapidly followed by extinction within 20 years (pink ribbon). However, even when testing high random juvenile mortality (blue ribbon) of 80%, most simulations still showed rapidly eroding genetic diversity with the population likely going extinct in 20 years, too.

In brief, the PVA analyses showed that, regardless of mortality rates, non-random mortality amongst sibling parrots always resulted in decreased population genetic diversity. Obviously, the key here is solving the pressing problem of high sibling mortalities. But the reasons underlying this high juvenile mortality remain unknown.

“I have a few theories”, Dr Stojanovic elaborated in email. “For example some of my earlier work shows that different OBP mothers (and lineages) tend to consistently produce heavier or lighter young, but we’ve not yet been able to directly attribute body mass to survival. It’s possible also that there’s some kind of shared early life experience that might affect siblings within a brood (e.g. poor parental care) but again, you’d expect this to equate to low body mass=low survival, but that’s not yet been demonstrable. It could also be some genetic factor, but individual level genetic factors that might explain survival in OBPs remain unstudied. So in short, we don’t really know, but there’s a range of potential explanations that we plan to test in coming years.”

What has been done so far to examine high juvenile mortality amongst siblings?

“There’s been a range of conservation interventions trialled over time, but unfortunately evaluating their individual benefits for the population is hard because every action is confounded in some way with another action or time (i.e. multiple actions are implemented each year on the entire population – this makes it hard to attribute success/failure to any one action)”, Dr Stojanovic continued in email. “A few years ago there was effort to ‘ranch’ mothers (where captive bred mothers were released in spring, allowed to breed in the wild, and then recaptured again before they migrate away).”

But in a recent study (ref), Dr Stojanovic and his collaborators found that even this unusual ‘ranch’ strategy of encouraging repeated breeding of captive-bred parrot mothers in the wild didn’t improve the odds of lineage survival.

This grim news is a powerful warning that emphasizes the need for conservation biologists to be constantly attentive to invisible threats, such as loss of family lineages within tiny populations, and to gather and analyse the relevant data so these scenarios can be dealt with early to avoid irreversible genetic damage to populations.

“It highlighted to me that conservation practitioners need to be constantly vigilant to these kinds of threats – which are surprisingly difficult to detect”, Dr Stojanovic said in email.

Orange-bellied parrots are an important case study for how reproductive skew can imperil a tiny conserved population and what can be done to address this issue.

“These parrots show us the value of collecting detailed monitoring data, but more importantly, they demonstrate the need to regularly evaluate demographic processes in small populations”, Dr Stojanovic told me in email.

“If we’d had this information 20 years ago, it’s likely OBPs would be in a much better place because maybe we could have preserved some of the genetic diversity that has now been permanently lost.”

Source:

Dejan Stojanovic, Teresa Neeman, Robert Lacy, Katherine A. Farquharson, Carolyn J. Hogg, and Robert Heinsohn (2022). Effects of non-random juvenile mortality on small, inbred populations, Biological Conservation 268:109504 | doi:10.1016/j.biocon.2022.109504

NOTE: This study was funded, in part, by a crowd-funding campaign (‘Operation OBP’) to which I contributed.

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