Genetic Management of Fragmented Animal and Plant Populations

10 12 2016

logoThat is the title of a new textbook that will be available mid-2017.

After almost 6 years work, authors Dick Frankham, Jonathan Ballou, Katherine Ralls, Mark Eldridge, Michele Dudash, Charles Fenster, Bob Lacy & Paul Sunnucks have produced an advanced textbook/research monograph that aims to provoke a paradigm shift in the management of small, isolated population fragments of animals and plants.

One of the greatest unmet challenges in conservation biology is the genetic management of fragmented populations of threatened animal and plant species. More than a million small, isolated, population fragments of threatened species are likely suffering inbreeding depression, loss of evolutionary potential, and elevated extinction risks (genetic erosion). Re-establishing gene flow between populations is required to reverse these effects, but managers very rarely do this. On the contrary, molecular genetic methods are mainly being used to document genetic differentiation among populations, with most studies concluding that genetically differentiated populations should be managed separately (i.e., kept isolated), thereby dooming many populations to eventual extinction.

The need for a paradigm shift in genetic management of fragmented populations has been highlighted as a major issue in conservation. The rapidly advancing field of molecular genetics is continually providing new tools to measure the extent of population fragmentation and its genetic consequences. However, adequate guidance on how to use these data for effective conservation is still lacking, and many populations are going extinct principally for genetic reasons. Consequently, there is now urgent need for an authoritative textbook on the subject.

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Food for sex

18 03 2013
Quercus_KakFeed Photo
Kakapo are unique among the ~ 400 parrot species (Psittaciformes) for being flightless, nocturnal and extremely long-lived (up to 100 years!). Additionally, they are herbivorous (seeds, fruits, polen, plants), males can weigh up to 2-4 kg (40% heavier than females), and females lay their eggs on the ground or cavities – i.e., 3 eggs in a single clutch annually, although 2 clutches might occur if the nest fails at the beginning of the reproductive season or if the eggs are taken for artificial incubation.Native to New Zealand, kakapo once inhabited the subalpine fringes of forest and scrub. Polynesians (1000 years ago) and Europeans (mostly in the XIX Century) arrived in the archipelago accompanied by dogs, cats, rats and mustelids that cornered kakapo populations in the Fiordland region (south-west of the South Island) where it was declared extinct in 1989. In 1977, a population of some 200 individuals was found on Stewart Island – this population was already in decline to the claws and jaws of feral cats. By the 1980s, the failure of captive breeding programs prompted the transfer of 60 individuals from Steward to carnivore-free islands. The global (known) population ‘rocketed’ from 50 individuals in 1999 to 126 in the 2012 censuses and, consequently, the kakapo’s IUCN status changed in 2000 from ‘Extinct in the Wild’ to ‘Critically Endangered’. Under the management of the Kakapo Recovery Programme, kakapo are now present on the islands of CodfishAnchor and Little Barrier.

Inbreeding, system shocks caused by fire or cyclones (for example), or demographic stochasticity (by which two or more outcomes are possible) such as how many males and females will be born in a single year, are all factors that threaten the persistence of small and fragmented populations. They can, however, be reverted by conservation actions.

If you have ever taken dancing classes, you will be familiar with the scarcity of male partners and how this can jeopardize group learning. When reproduction, rather than salsa pirouettes, is at stake, a biased sex ratio can compromise the persistence of species. For instance, when females are unable to find males (or vice versa), fertility rates can collapse as a result – a well-known cause of an Allee effect (1). Curiously, natural selection can promote such bias by favouring a species’ investment in litters dominated by one of the two genders. The evolutionary formulation of such scenario is that females can adjust the sex ratio of their offspring depending on the amount of available resources (2) – see contrasting cross-taxa studies on this subject (3-5). Thus, when resources abound (e.g., food), mothers can afford the offspring’s gender requiring more resources to reach adulthood or once adulthood is reached, is less likely to reproduce successfully (6). This predisposition to one gender or another can be key to the conservation of endangered species (7).

The kakapo case

At the end of the 1990s, the New Zealand Department of Conservation placed dispensers of supplementary food in the territories of some kakapo (a rather enormous, flightless parrot Strigops habroptilus) to encourage their reproduction. Back then, only 60 individuals were left of the entire species . Unfortunately, those females with access to the supplemental food conceived 67% of male chicks (so exacerbating the fact that kakapo populations are naturally male-biased), while those females without extra feeding had 71% of female chicks (8). Something wasn’t working. Read the rest of this entry »

De-extinction is about as sensible as de-death

15 03 2013

Published simultaneously in The Conversation.

On Friday, March 15 in Washington DC, National Geographic and TEDx are hosting a day-long conference on species-revival science and ethics. In other words, they will be debating whether we can, and should, attempt to bring extinct animals back to life – a concept some call “de-extinction”.

The debate has an interesting line-up of ecologists, geneticists, palaeontologists (including Australia’s own Mike Archer), developmental biologists, journalists, lawyers, ethicists and even artists. I have no doubt it will be very entertaining.

But let’s not mistake entertainment for reality. It disappoints me, a conservation scientist, that this tired fantasy still manages to generate serious interest. I have little doubt what the ecologists at the debate will conclude.

Once again, it’s important to discuss the principal flaws in such proposals.

Put aside for the moment the astounding inefficiency, the lack of success to date and the welfare issues of bringing something into existence only to suffer a short and likely painful life. The principal reason we should not even consider the technology from a conservation perspective is that it does not address the real problem – mainly, the reason for extinction in the first place.

Even if we could solve all the other problems, if there is no place to put these new individuals, the effort and money expended is a complete waste. Habitat loss is the principal driver of species extinction and endangerment. If we don’t stop and reverse this now, all other avenues are effectively closed. Cloning will not create new forests or coral reefs, for example. Read the rest of this entry »

Translocations: the genetic rescue paradox

14 01 2013

helphindranceHarvesting and habitat alteration reduce many populations to just a few individuals, and then often extinction. A widely recommended conservation action is to supplement those populations with new individuals translocated from other regions. However, crossing local and foreign genes can worsen the prospects of recovery.

We are all hybrids or combinations of other people, experiences and things. Let’s think of teams (e.g., engineers, athletes, mushroom collectors). In team work, isolation from other team members might limit the appearance of innovative ideas, but the arrival of new (conflictive) individuals might in fact destroy group dynamics altogether. Chromosomes work much like this – too little or too much genetic variability among parents can break down the fitness of their descendants. These pernicious effects are known as ‘inbreeding depression‘ when they result from reproduction among related individuals, and ‘outbreeding depression‘ when parents are too genetically distant.

CB_OutbreedingDepression Photo
Location of the two USA sites providing spawners of largemouth bass for the experiments by Goldberg et al. (3): the Kaskaskia River (Mississipi Basin, Illinois) and the Big Cedar Lake (Great Lakes Basin, Wisconsin). Next to the map is shown an array of three of the 72-litre aquaria in an indoor environment under constant ambient temperature (25 ◦C), humidity (60%), and photoperiod (alternate 12 hours of light and darkness). Photo courtesy of T. Goldberg.

Recent studies have revised outbreeding depression in a variety of plants, invertebrates and vertebrates (1, 2). An example is Tony Goldberg’s experiments on largemouth bass (Micropterus salmoides), a freshwater fish native to North America. Since the 1990s, the USA populations have been hit by disease from a Ranavirus. Goldberg et al. (3) sampled healthy individuals from two freshwater bodies: the Mississipi River and the Great Lakes, and created two genetic lineages by having both populations isolated and reproducing in experimental ponds. Then, they inoculated the Ranavirus in a group of parents from each freshwater basin (generation P), and in the first (G1) and second (G2) generations of hybrids crossed from both basins. After 3 weeks in experimental aquaria, the proportion of survivors declined to nearly 30% in G2, and exceeded 80% in G1 and P. Clearly, crossing of different genetic lineages increased the susceptibility of this species to a pathogen, and the impact was most deleterious in G2. This investigation indicates that translocation of foreign individuals into a self-reproducing population can not only import diseases, but also weaken its descendants’ resistance to future epidemics.

A mechanism causing outbreeding depression occurs when hybridisation alters a gene that is only functional in combination with other genes. Immune systems are often regulated by these complexes of co-adapted genes (‘supergenes’) and their disruption is a potential candidate for the outbreeding depression reported by Goldberg et al. (3). Along with accentuating susceptibility to disease, outbreeding depression in animals and plants can cause a variety of deleterious effects such as dwarfism, low fertility, or shortened life span. Dick Frankham (one of our collaborators) has quantified that the probability of outbreeding depression increases when mixing takes place between (i) different species, (ii) conspecifics adapted to different habitats, (iii) conspecifics with fixed chromosomal differences, and (iv) populations free of genetic flow with other populations for more than 500 years (2).

A striking example supporting (some of) those criteria is the pink salmon (Oncorhynchus gorbuscha) from Auke Creek near Juneau (Alaska). The adults migrate from the Pacific to their native river where they spawn two years after birth, with the particularity that there are two strict broodlines that spawn in either even or odd year – that is, the same species in the same river, but with a lack of genetic flow between populations. In vitro mixture of the two broodlines and later release of hybrids in the wild have shown that the second generation of hybrids had nearly 50% higher mortality rates (i.e., failure to return to spawn following release) when born from crossings of parents from different broodlines than when broodlines were not mixed (4).

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Ecology is a Tower of Babel

17 09 2012

The term ‘ecology’ in 16 different languages overlaid on the oil on board ‘The Tower of Babel’ by Flemish Renaissance painter Pieter Bruegel the Elder (1563).

In his song ‘Balada de Babel’, the Spanish artist Luis Eduardo Aute sings several lyrics in unison with the same melody. The effect is a wonderful mess. This is what the scientific literature sounds like when authors generate synonymies (equivalent meaning) and polysemies (multiple meanings), or coin terms to show a point of view. In our recent paper published in Oecologia, we illustrate this problem with regard to ‘density dependence’: a key ecological concept. While the biblical reference is somewhat galling to our atheist dispositions, the analogy is certainly appropriate.

A giant shoal of herring zigzagging in response to a predator; a swarm of social bees tending the multitudinous offspring of their queen; a dense pine forest depriving its own seedlings from light; an over-harvested population of lobsters where individuals can hardly find reproductive mates; pioneering strands of a seaweed colonising a foreign sea after a transoceanic trip attached to the hulk of boat; respiratory parasites spreading in a herd of caribou; or malaria protozoans making their way between mosquitoes and humans – these are all examples of population processes that operate under a density check. The number of individuals within those groups of organisms determines their chances for reproduction, survival or dispersal, which we (ecologists) measure as ‘demographic rates’ (e.g., number of births per mother, number of deaths between consecutive years, or number of immigrants per hectare).

In ecology, the causal relationship between the size of a population and a demographic rate is known as ‘density dependence’ (DD hereafter). This relationship captures the pace at which a demographic rate changes as population size varies in time and/or space. We use DD measurements to infer the operation of social and trophic interactions (cannibalism, competition, cooperation, disease, herbivory, mutualism, parasitism, parasitoidism, predation, reproductive behaviour and the like) between individuals within a population1,2, because the intensity of these interactions varies with population size. Thus, as a population of caribou expands, respiratory parasites will have an easier job to disperse from one animal to another. As the booming parasites breed, increased infestations will kill the weakest caribou or reduce the fertility of females investing too much energy to counteract the infection (yes, immunity is energetically costly, which is why you get sick when you are run down). In turn, as the caribou population decreases, so does the population of parasites3. In cybernetics, such a toing-and-froing is known as ‘feedback’ (a system that controls itself, like a thermostat controls the temperature of a room) – a ‘density feedback’ (Figure 1) is the kind we are highlighting here. Read the rest of this entry »

Ghosts of bottlenecks past

25 05 2012

© D. Bathory

I’ve just spent the last week at beautiful Linnaeus Estate on the northern NSW coast for my third Australian Centre for Ecological Analysis and Synthesis (ACEAS) (see previous post about my last ACEAS workshop).

This workshop is a little different to my last one, and I’m merely a participant (not the organiser) this time. Alan Cooper and members of his Australian Centre for Ancient DNA (Jeremy Austin, Vicki Thomson & Julien Soubrier) combined forces this week with Craig Mortiz, Margaret Byrne, Steve Donnellan, Tania Laity, Leo Joseph, Xander Xue and Gabriele Cybis. Our task was to examine the mounting evidence that many Australian species appear to show a rather shallow genetic pool from a (or several) major past bottlenecks.

What’s a ‘bottleneck’? In reference to the form after which it was named, a genetic bottleneck is the genetic diversity aftermath after a population declines to a small size and then later expands. The history of this reduction and subsequent expansion is written in the DNA, because inevitably gene ‘types’ are lost as most individuals shuffle off this mortal coil. In a way, it’s like losing a large population of people who all speak different languages – inevitably, you’d lose entire languages and the recovering population would grow out of a reduced ‘pool’ of languages, resulting in fewer overall surviving languages.

Our workshop focus started, as many scientific endeavours do, rather serendipitously. Several years ago, Jeremy Austin noticed that devils who had died out on the mainland several thousand years ago had a very low genetic diversity, as do modern-day devils surviving in Tasmania. He thought it was odd because they should have had more on the mainland given that was their principal distribution prior to Europeans arriving. He mentioned this in passing to Steve Donnellan one day and Steve announced that he had seem the same pattern in echidnas. Now, echidnas cover most of Australia’s surface, so that was equally odd. Then they decided to look at another widespread species – tiger snakes, emus, etc. – and found in many of them, the same patterns were there. Read the rest of this entry »

Tentacles of destruction

5 04 2012

This last post before Easter is something I’ve thought more and more about over the last few years. I wouldn’t have given it much time in the past, but I’m now convinced roads are one of the humanity’s most destructive devices. Let me explain.

Before I had a good grasp of extinction dynamics, I wouldn’t have attributed much import to the role of roads in conservation. I mean, really, a little road here and there (ok, even a major motorway) couldn’t possibly be a problem? It’s mostly habitat destruction itself, right?

Not exactly. With our work on extinction synergies, I eventually came to realise that roads are some of the first portals to the devastation to come. Read the rest of this entry »